diff --git a/sandbox/OpenIddict.Sandbox.AspNet.Client/Startup.cs b/sandbox/OpenIddict.Sandbox.AspNet.Client/Startup.cs
index ef1a8b16..ce75bc16 100644
--- a/sandbox/OpenIddict.Sandbox.AspNet.Client/Startup.cs
+++ b/sandbox/OpenIddict.Sandbox.AspNet.Client/Startup.cs
@@ -22,7 +22,7 @@ namespace OpenIddict.Sandbox.AspNet.Client
             // Register the Autofac scope injector middleware.
             app.UseAutofacLifetimeScopeInjector(container);
 
-            // Register the cookie middleware responsible of storing the user sessions.
+            // Register the cookie middleware responsible for storing the user sessions.
             app.UseCookieAuthentication(new CookieAuthenticationOptions
             {
                 ExpireTimeSpan = TimeSpan.FromMinutes(50),
diff --git a/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.Authentication.cs b/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.Authentication.cs
index 6e0f32ef..89454951 100644
--- a/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.Authentication.cs
+++ b/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.Authentication.cs
@@ -33,6 +33,7 @@ public static partial class OpenIddictClientOwinHandlers
              * Redirection response handling:
              */
             AttachHttpResponseCode<ApplyRedirectionResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyRedirectionResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyRedirectionResponseContext>.Descriptor,
             ProcessPassthroughErrorResponse<ApplyRedirectionResponseContext, RequireRedirectionEndpointPassthroughEnabled>.Descriptor,
             ProcessLocalErrorResponse<ApplyRedirectionResponseContext>.Descriptor);
diff --git a/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.cs b/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.cs
index 5b39ea4b..d19b8f6a 100644
--- a/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.cs
+++ b/src/OpenIddict.Client.Owin/OpenIddictClientOwinHandlers.cs
@@ -616,6 +616,58 @@ public static partial class OpenIddictClientOwinHandlers
         }
     }
 
+    /// <summary>
+    /// Contains the logic responsible for attaching an OWIN response chalenge to the context, if necessary.
+    /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
+    /// </summary>
+    public class AttachOwinResponseChallenge<TContext> : IOpenIddictClientHandler<TContext> where TContext : BaseRequestContext
+    {
+        /// <summary>
+        /// Gets the default descriptor definition assigned to this handler.
+        /// </summary>
+        public static OpenIddictClientHandlerDescriptor Descriptor { get; }
+            = OpenIddictClientHandlerDescriptor.CreateBuilder<TContext>()
+                .AddFilter<RequireOwinRequest>()
+                .UseSingletonHandler<AttachOwinResponseChallenge<TContext>>()
+                .SetOrder(AttachHttpResponseCode<TContext>.Descriptor.Order + 1_000)
+                .SetType(OpenIddictClientHandlerType.BuiltIn)
+                .Build();
+
+        /// <inheritdoc/>
+        public ValueTask HandleAsync(TContext context)
+        {
+            if (context is null)
+            {
+                throw new ArgumentNullException(nameof(context));
+            }
+
+            // This handler only applies to OWIN requests. If The OWIN request cannot be resolved,
+            // this may indicate that the request was incorrectly processed by another server stack.
+            var response = context.Transaction.GetOwinRequest()?.Context.Response ??
+                throw new InvalidOperationException(SR.GetResourceString(SR.ID0120));
+
+            // OWIN authentication middleware configured to use active authentication (which is the default mode)
+            // are known to aggressively intercept 401 responses even if the request is already considered fully
+            // handled. In practice, this behavior is often seen with the cookies authentication middleware,
+            // that will rewrite the 401 responses returned by OpenIddict and try to redirect the user agent
+            // to the login page configured in the options. To prevent this undesirable behavior, a fake
+            // response challenge pointing to a non-existent middleware is manually added to the OWIN context
+            // to prevent the active authentication middleware from rewriting OpenIddict's 401 HTTP responses.
+            //
+            // Note: while 403 responses are generally not intercepted by the built-in OWIN authentication
+            // middleware, they are treated the same way as 401 responses to account for custom middleware
+            // that may potentially use the same interception logic for both 401 and 403 HTTP responses.
+            if (response.StatusCode is 401 or 403 &&
+                response.Context.Authentication.AuthenticationResponseChallenge is null)
+            {
+                response.Context.Authentication.AuthenticationResponseChallenge =
+                    new AuthenticationResponseChallenge(new[] { Guid.NewGuid().ToString() }, null);
+            }
+
+            return default;
+        }
+    }
+
     /// <summary>
     /// Contains the logic responsible for attaching the appropriate HTTP response cache headers.
     /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
@@ -629,7 +681,7 @@ public static partial class OpenIddictClientOwinHandlers
             = OpenIddictClientHandlerDescriptor.CreateBuilder<TContext>()
                 .AddFilter<RequireOwinRequest>()
                 .UseSingletonHandler<AttachCacheControlHeader<TContext>>()
-                .SetOrder(AttachHttpResponseCode<TContext>.Descriptor.Order + 1_000)
+                .SetOrder(AttachOwinResponseChallenge<TContext>.Descriptor.Order + 1_000)
                 .SetType(OpenIddictClientHandlerType.BuiltIn)
                 .Build();
 
diff --git a/src/OpenIddict.Server.AspNetCore/OpenIddictServerAspNetCoreHandlers.cs b/src/OpenIddict.Server.AspNetCore/OpenIddictServerAspNetCoreHandlers.cs
index 599de079..e5d2e89f 100644
--- a/src/OpenIddict.Server.AspNetCore/OpenIddictServerAspNetCoreHandlers.cs
+++ b/src/OpenIddict.Server.AspNetCore/OpenIddictServerAspNetCoreHandlers.cs
@@ -37,6 +37,7 @@ public static partial class OpenIddictServerAspNetCoreHandlers
         /*
          * Challenge processing:
          */
+        AttachHostChallengeError.Descriptor,
         ResolveHostChallengeParameters.Descriptor,
 
         /*
@@ -277,11 +278,10 @@ public static partial class OpenIddictServerAspNetCoreHandlers
     }
 
     /// <summary>
-    /// Contains the logic responsible for resolving the additional sign-in parameters stored in the ASP.NET
-    /// Core authentication properties specified by the application that triggered the sign-in operation.
+    /// Contains the logic responsible for attaching the error details using the ASP.NET Core authentication properties.
     /// Note: this handler is not used when the OpenID Connect request is not initially handled by ASP.NET Core.
     /// </summary>
-    public class ResolveHostChallengeParameters : IOpenIddictServerHandler<ProcessChallengeContext>
+    public class AttachHostChallengeError : IOpenIddictServerHandler<ProcessChallengeContext>
     {
         /// <summary>
         /// Gets the default descriptor definition assigned to this handler.
@@ -289,7 +289,7 @@ public static partial class OpenIddictServerAspNetCoreHandlers
         public static OpenIddictServerHandlerDescriptor Descriptor { get; }
             = OpenIddictServerHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
                 .AddFilter<RequireHttpRequest>()
-                .UseSingletonHandler<ResolveHostChallengeParameters>()
+                .UseSingletonHandler<AttachHostChallengeError>()
                 .SetOrder(AttachDefaultChallengeError.Descriptor.Order - 500)
                 .SetType(OpenIddictServerHandlerType.BuiltIn)
                 .Build();
@@ -303,33 +303,48 @@ public static partial class OpenIddictServerAspNetCoreHandlers
             }
 
             var properties = context.Transaction.GetProperty<AuthenticationProperties>(typeof(AuthenticationProperties).FullName!);
-            if (properties is null)
+            if (properties is not null)
             {
-                return default;
+                context.Response.Error = properties.GetString(Properties.Error);
+                context.Response.ErrorDescription = properties.GetString(Properties.ErrorDescription);
+                context.Response.ErrorUri = properties.GetString(Properties.ErrorUri);
+                context.Response.Scope = properties.GetString(Properties.Scope);
             }
 
-            if (properties.Items.TryGetValue(Properties.Error, out string? error) &&
-                !string.IsNullOrEmpty(error))
-            {
-                context.Parameters[Parameters.Error] = error;
-            }
+            return default;
+        }
+    }
 
-            if (properties.Items.TryGetValue(Properties.ErrorDescription, out string? description) &&
-                !string.IsNullOrEmpty(description))
-            {
-                context.Parameters[Parameters.ErrorDescription] = description;
-            }
+    /// <summary>
+    /// Contains the logic responsible for resolving the additional sign-in parameters stored in the ASP.NET
+    /// Core authentication properties specified by the application that triggered the sign-in operation.
+    /// Note: this handler is not used when the OpenID Connect request is not initially handled by ASP.NET Core.
+    /// </summary>
+    public class ResolveHostChallengeParameters : IOpenIddictServerHandler<ProcessChallengeContext>
+    {
+        /// <summary>
+        /// Gets the default descriptor definition assigned to this handler.
+        /// </summary>
+        public static OpenIddictServerHandlerDescriptor Descriptor { get; }
+            = OpenIddictServerHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
+                .AddFilter<RequireHttpRequest>()
+                .UseSingletonHandler<ResolveHostChallengeParameters>()
+                .SetOrder(AttachChallengeParameters.Descriptor.Order - 500)
+                .SetType(OpenIddictServerHandlerType.BuiltIn)
+                .Build();
 
-            if (properties.Items.TryGetValue(Properties.ErrorUri, out string? uri) &&
-                !string.IsNullOrEmpty(uri))
+        /// <inheritdoc/>
+        public ValueTask HandleAsync(ProcessChallengeContext context)
+        {
+            if (context is null)
             {
-                context.Parameters[Parameters.ErrorUri] = uri;
+                throw new ArgumentNullException(nameof(context));
             }
 
-            if (properties.Items.TryGetValue(Properties.Scope, out string? scope) &&
-                !string.IsNullOrEmpty(scope))
+            var properties = context.Transaction.GetProperty<AuthenticationProperties>(typeof(AuthenticationProperties).FullName!);
+            if (properties is null)
             {
-                context.Parameters[Parameters.Scope] = scope;
+                return default;
             }
 
             foreach (var parameter in properties.Parameters)
@@ -875,29 +890,37 @@ public static partial class OpenIddictServerAspNetCoreHandlers
                 throw new ArgumentNullException(nameof(context));
             }
 
+            Debug.Assert(context.Transaction.Response is not null, SR.GetResourceString(SR.ID4007));
+
             // This handler only applies to ASP.NET Core requests. If the HTTP context cannot be resolved,
             // this may indicate that the request was incorrectly processed by another server stack.
             var response = context.Transaction.GetHttpRequest()?.HttpContext.Response ??
                 throw new InvalidOperationException(SR.GetResourceString(SR.ID0114));
 
-            Debug.Assert(context.Transaction.Response is not null, SR.GetResourceString(SR.ID4007));
-
-            // When client authentication is made using basic authentication, the authorization server MUST return
-            // a 401 response with a valid WWW-Authenticate header containing the Basic scheme and a non-empty realm.
-            // A similar error MAY be returned even when basic authentication is not used and MUST also be returned
-            // when an invalid token is received by the userinfo endpoint using the Bearer authentication scheme.
-            // To simplify the logic, a 401 response with the Bearer scheme is returned for invalid_token errors
-            // and a 401 response with the Basic scheme is returned for invalid_client, even if the credentials
-            // were specified in the request form instead of the HTTP headers, as allowed by the specification.
-            response.StatusCode = context.Transaction.Response.Error switch
+            response.StatusCode = (context.EndpointType, context.Transaction.Response.Error) switch
             {
-                null => 200, // Note: the default code may be replaced by another handler (e.g when doing redirects).
+                // Note: the default code may be replaced by another handler (e.g when doing redirects).
+                (_, null or { Length: 0 }) => 200,
+
+                // Unlike other server endpoints, errors returned by the userinfo endpoint follow the same logic as
+                // errors returned by API endpoints implementing bearer token authentication and MUST be returned
+                // as part of the standard WWW-Authenticate header. For more information, see
+                // https://openid.net/specs/openid-connect-core-1_0.html#UserInfoError.
+                (OpenIddictServerEndpointType.Userinfo, Errors.InvalidToken       or Errors.MissingToken)      => 401,
+                (OpenIddictServerEndpointType.Userinfo, Errors.InsufficientAccess or Errors.InsufficientScope) => 403,
 
-                Errors.InvalidClient or Errors.InvalidToken or Errors.MissingToken => 401,
+                // When client authentication is made using basic authentication, the authorization server
+                // MUST return a 401 response with a valid WWW-Authenticate header containing the HTTP Basic
+                // authentication scheme. A similar error MAY be returned even when using client_secret_post.
+                // To simplify the logic, a 401 response with the Basic scheme is returned for invalid_client
+                // errors, even if credentials were specified in the form, as allowed by the specification.
+                (not OpenIddictServerEndpointType.Userinfo, Errors.InvalidClient) => 401,
 
-                Errors.InsufficientAccess or Errors.InsufficientScope => 403,
+                (_, Errors.ServerError) => 500,
 
-                _  => 400
+                // Note: unless specified otherwise, errors are expected to result in 400 responses.
+                // See https://datatracker.ietf.org/doc/html/rfc6749#section-5.2 for more information.
+                _ => 400
             };
 
             return default;
@@ -973,29 +996,35 @@ public static partial class OpenIddictServerAspNetCoreHandlers
                 throw new ArgumentNullException(nameof(context));
             }
 
+            Debug.Assert(context.Transaction.Response is not null, SR.GetResourceString(SR.ID4007));
+
             // This handler only applies to ASP.NET Core requests. If the HTTP context cannot be resolved,
             // this may indicate that the request was incorrectly processed by another server stack.
             var response = context.Transaction.GetHttpRequest()?.HttpContext.Response ??
                 throw new InvalidOperationException(SR.GetResourceString(SR.ID0114));
 
-            Debug.Assert(context.Transaction.Response is not null, SR.GetResourceString(SR.ID4007));
+            if (string.IsNullOrEmpty(context.Transaction.Response.Error))
+            {
+                return default;
+            }
 
-            // When client authentication is made using basic authentication, the authorization server MUST return
-            // a 401 response with a valid WWW-Authenticate header containing the HTTP Basic authentication scheme.
-            // A similar error MAY be returned even when basic authentication is not used and MUST also be returned
-            // when an invalid token is received by the userinfo endpoint using the Bearer authentication scheme.
-            // To simplify the logic, a 401 response with the Bearer scheme is returned for invalid_token errors
-            // and a 401 response with the Basic scheme is returned for invalid_client, even if the credentials
-            // were specified in the request form instead of the HTTP headers, as allowed by the specification.
-            var scheme = context.Transaction.Response.Error switch
+            var scheme = (context.EndpointType, context.Transaction.Response.Error) switch
             {
-                Errors.InvalidClient => Schemes.Basic,
+                // Unlike other server endpoints, errors returned by the userinfo endpoint follow the same
+                // logic as errors returned by API endpoints implementing bearer token authentication and
+                // MUST be returned as part of the standard WWW-Authenticate header. For more information,
+                // see https://openid.net/specs/openid-connect-core-1_0.html#UserInfoError.
+                (OpenIddictServerEndpointType.Userinfo, _) => Schemes.Bearer,
 
-                Errors.InvalidToken or
-                Errors.MissingToken or
-                Errors.InsufficientAccess or
-                Errors.InsufficientScope => Schemes.Bearer,
+                // When client authentication is made using basic authentication, the authorization server
+                // MUST return a 401 response with a valid WWW-Authenticate header containing the HTTP Basic
+                // authentication scheme. A similar error MAY be returned even when using client_secret_post.
+                // To simplify the logic, a 401 response with the Basic scheme is returned for invalid_client
+                // errors, even if credentials were specified in the form, as allowed by the specification.
+                (_, Errors.InvalidClient) => Schemes.Basic,
 
+                // For all other errors, don't return a WWW-Authenticate header and return server errors
+                // as formatted JSON responses, as required by the OAuth 2.0 base specification.
                 _ => null
             };
 
@@ -1007,19 +1036,19 @@ public static partial class OpenIddictServerAspNetCoreHandlers
             var parameters = new Dictionary<string, string>(StringComparer.Ordinal);
 
             // If a realm was configured in the options, attach it to the parameters.
-            if (!string.IsNullOrEmpty(_options.CurrentValue.Realm))
+            if (_options.CurrentValue.Realm is string { Length: > 0 } realm)
             {
-                parameters[Parameters.Realm] = _options.CurrentValue.Realm;
+                parameters[Parameters.Realm] = realm;
             }
 
             foreach (var parameter in context.Transaction.Response.GetParameters())
             {
                 // Note: the error details are only included if the error was not caused by a missing token, as recommended
                 // by the OAuth 2.0 bearer specification: https://tools.ietf.org/html/rfc6750#section-3.1.
-                if (string.Equals(context.Transaction.Response.Error, Errors.MissingToken, StringComparison.Ordinal) &&
-                   (string.Equals(parameter.Key, Parameters.Error, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorDescription, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorUri, StringComparison.Ordinal)))
+                if (context.Transaction.Response.Error is Errors.MissingToken &&
+                    parameter.Key is Parameters.Error            or
+                                     Parameters.ErrorDescription or
+                                     Parameters.ErrorUri)
                 {
                     continue;
                 }
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Authentication.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Authentication.cs
index bc7cb726..b5184d45 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Authentication.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Authentication.cs
@@ -44,6 +44,7 @@ public static partial class OpenIddictServerOwinHandlers
              */
             RemoveCachedRequest.Descriptor,
             AttachHttpResponseCode<ApplyAuthorizationResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyAuthorizationResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyAuthorizationResponseContext>.Descriptor,
             ProcessFormPostResponse.Descriptor,
             ProcessQueryResponse.Descriptor,
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Device.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Device.cs
index 82bcd6d6..49fe072e 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Device.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Device.cs
@@ -25,6 +25,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Device response processing:
              */
             AttachHttpResponseCode<ApplyDeviceResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyDeviceResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyDeviceResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyDeviceResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyDeviceResponseContext>.Descriptor,
@@ -43,6 +44,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Verification response processing:
              */
             AttachHttpResponseCode<ApplyVerificationResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyVerificationResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyVerificationResponseContext>.Descriptor,
             ProcessHostRedirectionResponse.Descriptor,
             ProcessPassthroughErrorResponse<ApplyVerificationResponseContext, RequireVerificationEndpointPassthroughEnabled>.Descriptor,
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Discovery.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Discovery.cs
index 8cf2f73e..b7e76f9c 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Discovery.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Discovery.cs
@@ -22,6 +22,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Configuration response processing:
              */
             AttachHttpResponseCode<ApplyConfigurationResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyConfigurationResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyConfigurationResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyConfigurationResponseContext>.Descriptor,
 
@@ -34,6 +35,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Cryptography response processing:
              */
             AttachHttpResponseCode<ApplyCryptographyResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyCryptographyResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyCryptographyResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyCryptographyResponseContext>.Descriptor);
     }
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Exchange.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Exchange.cs
index 174ece72..8de80efd 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Exchange.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Exchange.cs
@@ -28,6 +28,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Token response processing:
              */
             AttachHttpResponseCode<ApplyTokenResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyTokenResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyTokenResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyTokenResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyTokenResponseContext>.Descriptor);
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Introspection.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Introspection.cs
index c9a7175e..9bd7a2d6 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Introspection.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Introspection.cs
@@ -23,6 +23,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Introspection response processing:
              */
             AttachHttpResponseCode<ApplyIntrospectionResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyIntrospectionResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyIntrospectionResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyIntrospectionResponseContext>.Descriptor);
     }
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Revocation.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Revocation.cs
index db85a8ac..94405ee1 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Revocation.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Revocation.cs
@@ -23,6 +23,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Revocation response processing:
              */
             AttachHttpResponseCode<ApplyRevocationResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyRevocationResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyRevocationResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyRevocationResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyRevocationResponseContext>.Descriptor);
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Session.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Session.cs
index c8f23b4e..1b15e441 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Session.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Session.cs
@@ -42,6 +42,7 @@ public static partial class OpenIddictServerOwinHandlers
              */
             RemoveCachedRequest.Descriptor,
             AttachHttpResponseCode<ApplyLogoutResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyLogoutResponseContext>.Descriptor,
             AttachCacheControlHeader<ApplyLogoutResponseContext>.Descriptor,
             ProcessHostRedirectionResponse.Descriptor,
             ProcessPassthroughErrorResponse<ApplyLogoutResponseContext, RequireLogoutEndpointPassthroughEnabled>.Descriptor,
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Userinfo.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Userinfo.cs
index 36cb6fb1..065ca209 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Userinfo.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.Userinfo.cs
@@ -28,6 +28,7 @@ public static partial class OpenIddictServerOwinHandlers
              * Userinfo response processing:
              */
             AttachHttpResponseCode<ApplyUserinfoResponseContext>.Descriptor,
+            AttachOwinResponseChallenge<ApplyUserinfoResponseContext>.Descriptor,
             AttachWwwAuthenticateHeader<ApplyUserinfoResponseContext>.Descriptor,
             ProcessChallengeErrorResponse<ApplyUserinfoResponseContext>.Descriptor,
             ProcessJsonResponse<ApplyUserinfoResponseContext>.Descriptor);
diff --git a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.cs b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.cs
index 409d88bf..90b3a968 100644
--- a/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.cs
+++ b/src/OpenIddict.Server.Owin/OpenIddictServerOwinHandlers.cs
@@ -32,7 +32,7 @@ public static partial class OpenIddictServerOwinHandlers
         /*
          * Challenge processing:
          */
-        ResolveHostChallengeParameters.Descriptor)
+        AttachHostChallengeError.Descriptor)
         .AddRange(Authentication.DefaultHandlers)
         .AddRange(Device.DefaultHandlers)
         .AddRange(Discovery.DefaultHandlers)
@@ -264,11 +264,10 @@ public static partial class OpenIddictServerOwinHandlers
     }
 
     /// <summary>
-    /// Contains the logic responsible for resolving the additional sign-in parameters stored in the OWIN
-    /// authentication properties specified by the application that triggered the sign-in operation.
+    /// Contains the logic responsible for attaching the error details using the OWIN authentication properties.
     /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
     /// </summary>
-    public class ResolveHostChallengeParameters : IOpenIddictServerHandler<ProcessChallengeContext>
+    public class AttachHostChallengeError : IOpenIddictServerHandler<ProcessChallengeContext>
     {
         /// <summary>
         /// Gets the default descriptor definition assigned to this handler.
@@ -276,8 +275,8 @@ public static partial class OpenIddictServerOwinHandlers
         public static OpenIddictServerHandlerDescriptor Descriptor { get; }
             = OpenIddictServerHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
                 .AddFilter<RequireOwinRequest>()
-                .UseSingletonHandler<ResolveHostChallengeParameters>()
-                .SetOrder(AttachChallengeParameters.Descriptor.Order - 500)
+                .UseSingletonHandler<AttachHostChallengeError>()
+                .SetOrder(AttachDefaultChallengeError.Descriptor.Order - 500)
                 .SetType(OpenIddictServerHandlerType.BuiltIn)
                 .Build();
 
@@ -290,36 +289,18 @@ public static partial class OpenIddictServerOwinHandlers
             }
 
             var properties = context.Transaction.GetProperty<AuthenticationProperties>(typeof(AuthenticationProperties).FullName!);
-            if (properties is null)
+            if (properties is not null)
             {
-                return default;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.Error, out string? error) &&
-                !string.IsNullOrEmpty(error))
-            {
-                context.Parameters[Parameters.Error] = error;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.ErrorDescription, out string? description) &&
-                !string.IsNullOrEmpty(description))
-            {
-                context.Parameters[Parameters.ErrorDescription] = description;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.ErrorUri, out string? uri) &&
-                !string.IsNullOrEmpty(uri))
-            {
-                context.Parameters[Parameters.ErrorUri] = uri;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.Scope, out string? scope) &&
-                !string.IsNullOrEmpty(scope))
-            {
-                context.Parameters[Parameters.Scope] = scope;
+                context.Response.Error = GetProperty(properties, Properties.Error);
+                context.Response.ErrorDescription = GetProperty(properties, Properties.ErrorDescription);
+                context.Response.ErrorUri = GetProperty(properties, Properties.ErrorUri);
+                context.Response.Scope = GetProperty(properties, Properties.Scope);
             }
 
             return default;
+
+            static string? GetProperty(AuthenticationProperties properties, string name)
+                => properties.Dictionary.TryGetValue(name, out string? value) ? value : null;
         }
     }
 
@@ -740,23 +721,83 @@ public static partial class OpenIddictServerOwinHandlers
             var response = context.Transaction.GetOwinRequest()?.Context.Response ??
                 throw new InvalidOperationException(SR.GetResourceString(SR.ID0120));
 
-            // When client authentication is made using basic authentication, the authorization server MUST return
-            // a 401 response with a valid WWW-Authenticate header containing the Basic scheme and a non-empty realm.
-            // A similar error MAY be returned even when basic authentication is not used and MUST also be returned
-            // when an invalid token is received by the userinfo endpoint using the Bearer authentication scheme.
-            // To simplify the logic, a 401 response with the Bearer scheme is returned for invalid_token errors
-            // and a 401 response with the Basic scheme is returned for invalid_client, even if the credentials
-            // were specified in the request form instead of the HTTP headers, as allowed by the specification.
-            response.StatusCode = context.Transaction.Response.Error switch
+            response.StatusCode = (context.EndpointType, context.Transaction.Response.Error) switch
             {
-                null => 200, // Note: the default code may be replaced by another handler (e.g when doing redirects).
+                // Note: the default code may be replaced by another handler (e.g when doing redirects).
+                (_, null or { Length: 0 }) => 200,
+
+                // Unlike other server endpoints, errors returned by the userinfo endpoint follow the same logic as
+                // errors returned by API endpoints implementing bearer token authentication and MUST be returned
+                // as part of the standard WWW-Authenticate header. For more information, see
+                // https://openid.net/specs/openid-connect-core-1_0.html#UserInfoError.
+                (OpenIddictServerEndpointType.Userinfo, Errors.InvalidToken       or Errors.MissingToken)      => 401,
+                (OpenIddictServerEndpointType.Userinfo, Errors.InsufficientAccess or Errors.InsufficientScope) => 403,
+
+                // When client authentication is made using basic authentication, the authorization server
+                // MUST return a 401 response with a valid WWW-Authenticate header containing the HTTP Basic
+                // authentication scheme. A similar error MAY be returned even when using client_secret_post.
+                // To simplify the logic, a 401 response with the Basic scheme is returned for invalid_client
+                // errors, even if credentials were specified in the form, as allowed by the specification.
+                (not OpenIddictServerEndpointType.Userinfo, Errors.InvalidClient) => 401,
+
+                (_, Errors.ServerError) => 500,
+
+                // Note: unless specified otherwise, errors are expected to result in 400 responses.
+                // See https://datatracker.ietf.org/doc/html/rfc6749#section-5.2 for more information.
+                _ => 400
+            };
 
-                Errors.InvalidClient or Errors.InvalidToken or Errors.MissingToken => 401,
+            return default;
+        }
+    }
 
-                Errors.InsufficientAccess or Errors.InsufficientScope => 403,
+    /// <summary>
+    /// Contains the logic responsible for attaching an OWIN response chalenge to the context, if necessary.
+    /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
+    /// </summary>
+    public class AttachOwinResponseChallenge<TContext> : IOpenIddictServerHandler<TContext> where TContext : BaseRequestContext
+    {
+        /// <summary>
+        /// Gets the default descriptor definition assigned to this handler.
+        /// </summary>
+        public static OpenIddictServerHandlerDescriptor Descriptor { get; }
+            = OpenIddictServerHandlerDescriptor.CreateBuilder<TContext>()
+                .AddFilter<RequireOwinRequest>()
+                .UseSingletonHandler<AttachOwinResponseChallenge<TContext>>()
+                .SetOrder(AttachHttpResponseCode<TContext>.Descriptor.Order + 1_000)
+                .SetType(OpenIddictServerHandlerType.BuiltIn)
+                .Build();
 
-                _ => 400
-            };
+        /// <inheritdoc/>
+        public ValueTask HandleAsync(TContext context)
+        {
+            if (context is null)
+            {
+                throw new ArgumentNullException(nameof(context));
+            }
+
+            // This handler only applies to OWIN requests. If The OWIN request cannot be resolved,
+            // this may indicate that the request was incorrectly processed by another server stack.
+            var response = context.Transaction.GetOwinRequest()?.Context.Response ??
+                throw new InvalidOperationException(SR.GetResourceString(SR.ID0120));
+
+            // OWIN authentication middleware configured to use active authentication (which is the default mode)
+            // are known to aggressively intercept 401 responses even if the request is already considered fully
+            // handled. In practice, this behavior is often seen with the cookies authentication middleware,
+            // that will rewrite the 401 responses returned by OpenIddict and try to redirect the user agent
+            // to the login page configured in the options. To prevent this undesirable behavior, a fake
+            // response challenge pointing to a non-existent middleware is manually added to the OWIN context
+            // to prevent the active authentication middleware from rewriting OpenIddict's 401 HTTP responses.
+            //
+            // Note: while 403 responses are generally not intercepted by the built-in OWIN authentication
+            // middleware, they are treated the same way as 401 responses to account for custom middleware
+            // that may potentially use the same interception logic for both 401 and 403 HTTP responses.
+            if (response.StatusCode is 401 or 403 &&
+                response.Context.Authentication.AuthenticationResponseChallenge is null)
+            {
+                response.Context.Authentication.AuthenticationResponseChallenge =
+                    new AuthenticationResponseChallenge(new[] { Guid.NewGuid().ToString() }, null);
+            }
 
             return default;
         }
@@ -775,7 +816,7 @@ public static partial class OpenIddictServerOwinHandlers
             = OpenIddictServerHandlerDescriptor.CreateBuilder<TContext>()
                 .AddFilter<RequireOwinRequest>()
                 .UseSingletonHandler<AttachCacheControlHeader<TContext>>()
-                .SetOrder(AttachHttpResponseCode<TContext>.Descriptor.Order + 1_000)
+                .SetOrder(AttachOwinResponseChallenge<TContext>.Descriptor.Order + 1_000)
                 .SetType(OpenIddictServerHandlerType.BuiltIn)
                 .Build();
 
@@ -838,22 +879,28 @@ public static partial class OpenIddictServerOwinHandlers
             var response = context.Transaction.GetOwinRequest()?.Context.Response ??
                 throw new InvalidOperationException(SR.GetResourceString(SR.ID0120));
 
-            // When client authentication is made using basic authentication, the authorization server MUST return
-            // a 401 response with a valid WWW-Authenticate header containing the HTTP Basic authentication scheme.
-            // A similar error MAY be returned even when basic authentication is not used and MUST also be returned
-            // when an invalid token is received by the userinfo endpoint using the Bearer authentication scheme.
-            // To simplify the logic, a 401 response with the Bearer scheme is returned for invalid_token errors
-            // and a 401 response with the Basic scheme is returned for invalid_client, even if the credentials
-            // were specified in the request form instead of the HTTP headers, as allowed by the specification.
-            var scheme = context.Transaction.Response.Error switch
+            if (string.IsNullOrEmpty(context.Transaction.Response.Error))
             {
-                Errors.InvalidClient => Schemes.Basic,
-
-                Errors.InvalidToken or
-                Errors.MissingToken or
-                Errors.InsufficientAccess or
-                Errors.InsufficientScope => Schemes.Bearer,
+                return default;
+            }
 
+            var scheme = (context.EndpointType, context.Transaction.Response.Error) switch
+            {
+                // Unlike other server endpoints, errors returned by the userinfo endpoint follow the same
+                // logic as errors returned by API endpoints implementing bearer token authentication and
+                // MUST be returned as part of the standard WWW-Authenticate header. For more information,
+                // see https://openid.net/specs/openid-connect-core-1_0.html#UserInfoError.
+                (OpenIddictServerEndpointType.Userinfo, _) => Schemes.Bearer,
+
+                // When client authentication is made using basic authentication, the authorization server
+                // MUST return a 401 response with a valid WWW-Authenticate header containing the HTTP Basic
+                // authentication scheme. A similar error MAY be returned even when using client_secret_post.
+                // To simplify the logic, a 401 response with the Basic scheme is returned for invalid_client
+                // errors, even if credentials were specified in the form, as allowed by the specification.
+                (_, Errors.InvalidClient) => Schemes.Basic,
+
+                // For all other errors, don't return a WWW-Authenticate header and return server errors
+                // as formatted JSON responses, as required by the OAuth 2.0 base specification.
                 _ => null
             };
 
@@ -865,19 +912,19 @@ public static partial class OpenIddictServerOwinHandlers
             var parameters = new Dictionary<string, string>(StringComparer.Ordinal);
 
             // If a realm was configured in the options, attach it to the parameters.
-            if (!string.IsNullOrEmpty(_options.CurrentValue.Realm))
+            if (_options.CurrentValue.Realm is string { Length: > 0 } realm)
             {
-                parameters[Parameters.Realm] = _options.CurrentValue.Realm;
+                parameters[Parameters.Realm] = realm;
             }
 
             foreach (var parameter in context.Transaction.Response.GetParameters())
             {
                 // Note: the error details are only included if the error was not caused by a missing token, as recommended
                 // by the OAuth 2.0 bearer specification: https://tools.ietf.org/html/rfc6750#section-3.1.
-                if (string.Equals(context.Transaction.Response.Error, Errors.MissingToken, StringComparison.Ordinal) &&
-                   (string.Equals(parameter.Key, Parameters.Error, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorDescription, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorUri, StringComparison.Ordinal)))
+                if (context.Transaction.Response.Error is Errors.MissingToken &&
+                    parameter.Key is Parameters.Error            or
+                                     Parameters.ErrorDescription or
+                                     Parameters.ErrorUri)
                 {
                     continue;
                 }
diff --git a/src/OpenIddict.Server/OpenIddictServerHandlers.cs b/src/OpenIddict.Server/OpenIddictServerHandlers.cs
index 70d8b13b..aa5cbf1e 100644
--- a/src/OpenIddict.Server/OpenIddictServerHandlers.cs
+++ b/src/OpenIddict.Server/OpenIddictServerHandlers.cs
@@ -907,47 +907,38 @@ public static partial class OpenIddictServerHandlers
                 throw new ArgumentNullException(nameof(context));
             }
 
-            if (!context.Parameters.ContainsKey(Parameters.Error))
+            context.Response.Error ??= context.EndpointType switch
             {
-                context.Parameters[Parameters.Error] = context.EndpointType switch
-                {
-                    OpenIddictServerEndpointType.Authorization or OpenIddictServerEndpointType.Verification
-                        => Errors.AccessDenied,
+                OpenIddictServerEndpointType.Authorization or OpenIddictServerEndpointType.Verification
+                    => Errors.AccessDenied,
 
-                    OpenIddictServerEndpointType.Token    => Errors.InvalidGrant,
-                    OpenIddictServerEndpointType.Userinfo => Errors.InsufficientAccess,
+                OpenIddictServerEndpointType.Token    => Errors.InvalidGrant,
+                OpenIddictServerEndpointType.Userinfo => Errors.InsufficientAccess,
 
-                    _ => throw new InvalidOperationException(SR.GetResourceString(SR.ID0006))
-                };
-            }
+                _ => throw new InvalidOperationException(SR.GetResourceString(SR.ID0006))
+            };
 
-            if (!context.Parameters.ContainsKey(Parameters.ErrorDescription))
+            context.Response.ErrorDescription ??= context.EndpointType switch
             {
-                context.Parameters[Parameters.ErrorDescription] = context.EndpointType switch
-                {
-                    OpenIddictServerEndpointType.Authorization or OpenIddictServerEndpointType.Verification
-                        => SR.GetResourceString(SR.ID2015),
+                OpenIddictServerEndpointType.Authorization or OpenIddictServerEndpointType.Verification
+                    => SR.GetResourceString(SR.ID2015),
 
-                    OpenIddictServerEndpointType.Token    => SR.GetResourceString(SR.ID2024),
-                    OpenIddictServerEndpointType.Userinfo => SR.GetResourceString(SR.ID2025),
+                OpenIddictServerEndpointType.Token    => SR.GetResourceString(SR.ID2024),
+                OpenIddictServerEndpointType.Userinfo => SR.GetResourceString(SR.ID2025),
 
-                    _ => throw new InvalidOperationException(SR.GetResourceString(SR.ID0006))
-                };
-            }
+                _ => throw new InvalidOperationException(SR.GetResourceString(SR.ID0006))
+            };
 
-            if (!context.Parameters.ContainsKey(Parameters.ErrorUri))
+            context.Response.ErrorUri ??= context.EndpointType switch
             {
-                context.Parameters[Parameters.ErrorUri] = context.EndpointType switch
-                {
-                    OpenIddictServerEndpointType.Authorization or OpenIddictServerEndpointType.Verification
-                        => SR.FormatID8000(SR.ID2015),
+                OpenIddictServerEndpointType.Authorization or OpenIddictServerEndpointType.Verification
+                    => SR.FormatID8000(SR.ID2015),
 
-                    OpenIddictServerEndpointType.Token    => SR.FormatID8000(SR.ID2024),
-                    OpenIddictServerEndpointType.Userinfo => SR.FormatID8000(SR.ID2025),
+                OpenIddictServerEndpointType.Token    => SR.FormatID8000(SR.ID2024),
+                OpenIddictServerEndpointType.Userinfo => SR.FormatID8000(SR.ID2025),
 
-                    _ => throw new InvalidOperationException(SR.GetResourceString(SR.ID0006))
-                };
-            }
+                _ => throw new InvalidOperationException(SR.GetResourceString(SR.ID0006))
+            };
 
             return default;
         }
diff --git a/src/OpenIddict.Validation.AspNetCore/OpenIddictValidationAspNetCoreHandlers.cs b/src/OpenIddict.Validation.AspNetCore/OpenIddictValidationAspNetCoreHandlers.cs
index 19ab53d0..5343057e 100644
--- a/src/OpenIddict.Validation.AspNetCore/OpenIddictValidationAspNetCoreHandlers.cs
+++ b/src/OpenIddict.Validation.AspNetCore/OpenIddictValidationAspNetCoreHandlers.cs
@@ -43,6 +43,7 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
          * Challenge processing:
          */
         AttachHostChallengeError.Descriptor,
+        ResolveHostChallengeParameters.Descriptor,
 
         /*
          * Response processing:
@@ -51,13 +52,16 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
         AttachCacheControlHeader<ProcessChallengeContext>.Descriptor,
         AttachWwwAuthenticateHeader<ProcessChallengeContext>.Descriptor,
         ProcessChallengeErrorResponse<ProcessChallengeContext>.Descriptor,
-        ProcessJsonResponse<ProcessChallengeContext>.Descriptor,
 
         AttachHttpResponseCode<ProcessErrorContext>.Descriptor,
         AttachCacheControlHeader<ProcessErrorContext>.Descriptor,
         AttachWwwAuthenticateHeader<ProcessErrorContext>.Descriptor,
-        ProcessChallengeErrorResponse<ProcessChallengeContext>.Descriptor,
-        ProcessJsonResponse<ProcessErrorContext>.Descriptor);
+        ProcessChallengeErrorResponse<ProcessErrorContext>.Descriptor,
+
+        /*
+         * Error processing:
+         */
+        AttachErrorParameters.Descriptor);
 
     /// <summary>
     /// Contains the logic responsible for infering the default issuer from the HTTP request host and validating it.
@@ -292,7 +296,7 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
             = OpenIddictValidationHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
                 .AddFilter<RequireHttpRequest>()
                 .UseSingletonHandler<AttachHostChallengeError>()
-                .SetOrder(int.MinValue + 50_000)
+                .SetOrder(AttachDefaultChallengeError.Descriptor.Order - 500)
                 .SetType(OpenIddictValidationHandlerType.BuiltIn)
                 .Build();
 
@@ -305,33 +309,48 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
             }
 
             var properties = context.Transaction.GetProperty<AuthenticationProperties>(typeof(AuthenticationProperties).FullName!);
-            if (properties is null)
+            if (properties is not null)
             {
-                return default;
+                context.Response.Error = properties.GetString(Properties.Error);
+                context.Response.ErrorDescription = properties.GetString(Properties.ErrorDescription);
+                context.Response.ErrorUri = properties.GetString(Properties.ErrorUri);
+                context.Response.Scope = properties.GetString(Properties.Scope);
             }
 
-            if (properties.Items.TryGetValue(Properties.Error, out string? error) &&
-                !string.IsNullOrEmpty(error))
-            {
-                context.Parameters[Parameters.Error] = error;
-            }
+            return default;
+        }
+    }
 
-            if (properties.Items.TryGetValue(Properties.ErrorDescription, out string? description) &&
-                !string.IsNullOrEmpty(description))
-            {
-                context.Parameters[Parameters.ErrorDescription] = description;
-            }
+    /// <summary>
+    /// Contains the logic responsible for resolving the additional sign-in parameters stored in the ASP.NET
+    /// Core authentication properties specified by the application that triggered the sign-in operation.
+    /// Note: this handler is not used when the OpenID Connect request is not initially handled by ASP.NET Core.
+    /// </summary>
+    public class ResolveHostChallengeParameters : IOpenIddictValidationHandler<ProcessChallengeContext>
+    {
+        /// <summary>
+        /// Gets the default descriptor definition assigned to this handler.
+        /// </summary>
+        public static OpenIddictValidationHandlerDescriptor Descriptor { get; }
+            = OpenIddictValidationHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
+                .AddFilter<RequireHttpRequest>()
+                .UseSingletonHandler<ResolveHostChallengeParameters>()
+                .SetOrder(AttachChallengeParameters.Descriptor.Order - 500)
+                .SetType(OpenIddictValidationHandlerType.BuiltIn)
+                .Build();
 
-            if (properties.Items.TryGetValue(Properties.ErrorUri, out string? uri) &&
-                !string.IsNullOrEmpty(uri))
+        /// <inheritdoc/>
+        public ValueTask HandleAsync(ProcessChallengeContext context)
+        {
+            if (context is null)
             {
-                context.Parameters[Parameters.ErrorUri] = uri;
+                throw new ArgumentNullException(nameof(context));
             }
 
-            if (properties.Items.TryGetValue(Properties.Scope, out string? scope) &&
-                !string.IsNullOrEmpty(scope))
+            var properties = context.Transaction.GetProperty<AuthenticationProperties>(typeof(AuthenticationProperties).FullName!);
+            if (properties is null)
             {
-                context.Parameters[Parameters.Scope] = scope;
+                return default;
             }
 
             foreach (var parameter in properties.Parameters)
@@ -391,12 +410,15 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
 
             response.StatusCode = context.Transaction.Response.Error switch
             {
-                null => 200,
+                // Note: the default code may be replaced by another handler (e.g when doing redirects).
+                null or { Length: 0 } => 200,
 
                 Errors.InvalidToken or Errors.MissingToken => 401,
 
                 Errors.InsufficientAccess or Errors.InsufficientScope => 403,
 
+                Errors.ServerError => 500,
+
                 _ => 400
             };
 
@@ -480,37 +502,34 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
             var response = context.Transaction.GetHttpRequest()?.HttpContext.Response ??
                 throw new InvalidOperationException(SR.GetResourceString(SR.ID0114));
 
-            var scheme = context.Transaction.Response.Error switch
-            {
-                Errors.InvalidToken or
-                Errors.MissingToken or
-                Errors.InsufficientAccess or
-                Errors.InsufficientScope => Schemes.Bearer,
-
-                _ => null
-            };
-
-            if (string.IsNullOrEmpty(scheme))
+            if (string.IsNullOrEmpty(context.Transaction.Response.Error))
             {
                 return default;
             }
 
+            // Note: unlike the server stack, the validation stack doesn't expose any endpoint
+            // and thus never returns responses containing a formatted body (e.g a JSON response).
+            //
+            // As such, all errors - even errors indicating an invalid request - are returned
+            // as part of the standard WWW-Authenticate header, as defined by the specification.
+            // See https://datatracker.ietf.org/doc/html/rfc6750#section-3 for more information.
+
             var parameters = new Dictionary<string, string>(StringComparer.Ordinal);
 
             // If a realm was configured in the options, attach it to the parameters.
-            if (!string.IsNullOrEmpty(_options.CurrentValue.Realm))
+            if (_options.CurrentValue.Realm is string { Length: > 0 } realm)
             {
-                parameters[Parameters.Realm] = _options.CurrentValue.Realm;
+                parameters[Parameters.Realm] = realm;
             }
 
             foreach (var parameter in context.Transaction.Response.GetParameters())
             {
                 // Note: the error details are only included if the error was not caused by a missing token, as recommended
                 // by the OAuth 2.0 bearer specification: https://tools.ietf.org/html/rfc6750#section-3.1.
-                if (string.Equals(context.Transaction.Response.Error, Errors.MissingToken, StringComparison.Ordinal) &&
-                   (string.Equals(parameter.Key, Parameters.Error, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorDescription, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorUri, StringComparison.Ordinal)))
+                if (context.Transaction.Response.Error is Errors.MissingToken &&
+                    parameter.Key is Parameters.Error            or
+                                     Parameters.ErrorDescription or
+                                     Parameters.ErrorUri)
                 {
                     continue;
                 }
@@ -525,7 +544,7 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
                 parameters[parameter.Key] = value;
             }
 
-            var builder = new StringBuilder(scheme);
+            var builder = new StringBuilder(Schemes.Bearer);
 
             foreach (var parameter in parameters)
             {
@@ -592,58 +611,4 @@ public static partial class OpenIddictValidationAspNetCoreHandlers
             return default;
         }
     }
-
-    /// <summary>
-    /// Contains the logic responsible for processing OpenID Connect responses that must be returned as JSON.
-    /// Note: this handler is not used when the OpenID Connect request is not initially handled by ASP.NET Core.
-    /// </summary>
-    public class ProcessJsonResponse<TContext> : IOpenIddictValidationHandler<TContext> where TContext : BaseRequestContext
-    {
-        /// <summary>
-        /// Gets the default descriptor definition assigned to this handler.
-        /// </summary>
-        public static OpenIddictValidationHandlerDescriptor Descriptor { get; }
-            = OpenIddictValidationHandlerDescriptor.CreateBuilder<TContext>()
-                .AddFilter<RequireHttpRequest>()
-                .UseSingletonHandler<ProcessJsonResponse<TContext>>()
-                .SetOrder(ProcessChallengeErrorResponse<TContext>.Descriptor.Order + 1_000)
-                .SetType(OpenIddictValidationHandlerType.BuiltIn)
-                .Build();
-
-        /// <inheritdoc/>
-        public async ValueTask HandleAsync(TContext context)
-        {
-            if (context is null)
-            {
-                throw new ArgumentNullException(nameof(context));
-            }
-
-            Debug.Assert(context.Transaction.Response is not null, SR.GetResourceString(SR.ID4007));
-
-            // This handler only applies to ASP.NET Core requests. If the HTTP context cannot be resolved,
-            // this may indicate that the request was incorrectly processed by another server stack.
-            var response = context.Transaction.GetHttpRequest()?.HttpContext.Response ??
-                throw new InvalidOperationException(SR.GetResourceString(SR.ID0114));
-
-            context.Logger.LogInformation(SR.GetResourceString(SR.ID6142), context.Transaction.Response);
-
-            using var stream = new MemoryStream();
-            using var writer = new Utf8JsonWriter(stream, new JsonWriterOptions
-            {
-                Encoder = JavaScriptEncoder.UnsafeRelaxedJsonEscaping,
-                Indented = true
-            });
-
-            context.Transaction.Response.WriteTo(writer);
-            writer.Flush();
-
-            response.ContentLength = stream.Length;
-            response.ContentType = "application/json;charset=UTF-8";
-
-            stream.Seek(offset: 0, loc: SeekOrigin.Begin);
-            await stream.CopyToAsync(response.Body, 4096, response.HttpContext.RequestAborted);
-
-            context.HandleRequest();
-        }
-    }
 }
diff --git a/src/OpenIddict.Validation.Owin/OpenIddictValidationOwinHandlers.cs b/src/OpenIddict.Validation.Owin/OpenIddictValidationOwinHandlers.cs
index 28433e01..6ce97fd0 100644
--- a/src/OpenIddict.Validation.Owin/OpenIddictValidationOwinHandlers.cs
+++ b/src/OpenIddict.Validation.Owin/OpenIddictValidationOwinHandlers.cs
@@ -43,16 +43,21 @@ public static partial class OpenIddictValidationOwinHandlers
          * Response processing:
          */
         AttachHttpResponseCode<ProcessChallengeContext>.Descriptor,
+        AttachOwinResponseChallenge<ProcessChallengeContext>.Descriptor,
         AttachCacheControlHeader<ProcessChallengeContext>.Descriptor,
         AttachWwwAuthenticateHeader<ProcessChallengeContext>.Descriptor,
         ProcessChallengeErrorResponse<ProcessChallengeContext>.Descriptor,
-        ProcessJsonResponse<ProcessChallengeContext>.Descriptor,
 
         AttachHttpResponseCode<ProcessErrorContext>.Descriptor,
+        AttachOwinResponseChallenge<ProcessErrorContext>.Descriptor,
         AttachCacheControlHeader<ProcessErrorContext>.Descriptor,
         AttachWwwAuthenticateHeader<ProcessErrorContext>.Descriptor,
         ProcessChallengeErrorResponse<ProcessErrorContext>.Descriptor,
-        ProcessJsonResponse<ProcessErrorContext>.Descriptor);
+
+        /*
+         * Error processing:
+         */
+        AttachErrorParameters.Descriptor);
 
     /// <summary>
     /// Contains the logic responsible for infering the default issuer from the HTTP request host and validating it.
@@ -289,7 +294,7 @@ public static partial class OpenIddictValidationOwinHandlers
             = OpenIddictValidationHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
                 .AddFilter<RequireOwinRequest>()
                 .UseSingletonHandler<AttachHostChallengeError>()
-                .SetOrder(int.MinValue + 50_000)
+                .SetOrder(AttachDefaultChallengeError.Descriptor.Order - 500)
                 .SetType(OpenIddictValidationHandlerType.BuiltIn)
                 .Build();
 
@@ -302,36 +307,18 @@ public static partial class OpenIddictValidationOwinHandlers
             }
 
             var properties = context.Transaction.GetProperty<AuthenticationProperties>(typeof(AuthenticationProperties).FullName!);
-            if (properties is null)
-            {
-                return default;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.Error, out string? error) &&
-                !string.IsNullOrEmpty(error))
-            {
-                context.Parameters[Parameters.Error] = error;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.ErrorDescription, out string? description) &&
-                !string.IsNullOrEmpty(description))
-            {
-                context.Parameters[Parameters.ErrorDescription] = description;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.ErrorUri, out string? uri) &&
-                !string.IsNullOrEmpty(uri))
+            if (properties is not null)
             {
-                context.Parameters[Parameters.ErrorUri] = uri;
-            }
-
-            if (properties.Dictionary.TryGetValue(Properties.Scope, out string? scope) &&
-                !string.IsNullOrEmpty(scope))
-            {
-                context.Parameters[Parameters.Scope] = scope;
+                context.Response.Error = GetProperty(properties, Properties.Error);
+                context.Response.ErrorDescription = GetProperty(properties, Properties.ErrorDescription);
+                context.Response.ErrorUri = GetProperty(properties, Properties.ErrorUri);
+                context.Response.Scope = GetProperty(properties, Properties.Scope);
             }
 
             return default;
+
+            static string? GetProperty(AuthenticationProperties properties, string name)
+                => properties.Dictionary.TryGetValue(name, out string? value) ? value : null;
         }
     }
 
@@ -369,12 +356,15 @@ public static partial class OpenIddictValidationOwinHandlers
 
             response.StatusCode = context.Transaction.Response.Error switch
             {
-                null => 200,
+                // Note: the default code may be replaced by another handler (e.g when doing redirects).
+                null or { Length: 0 } => 200,
 
                 Errors.InvalidToken or Errors.MissingToken => 401,
 
                 Errors.InsufficientAccess or Errors.InsufficientScope => 403,
 
+                Errors.ServerError => 500,
+
                 _ => 400
             };
 
@@ -382,6 +372,58 @@ public static partial class OpenIddictValidationOwinHandlers
         }
     }
 
+    /// <summary>
+    /// Contains the logic responsible for attaching an OWIN response chalenge to the context, if necessary.
+    /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
+    /// </summary>
+    public class AttachOwinResponseChallenge<TContext> : IOpenIddictValidationHandler<TContext> where TContext : BaseRequestContext
+    {
+        /// <summary>
+        /// Gets the default descriptor definition assigned to this handler.
+        /// </summary>
+        public static OpenIddictValidationHandlerDescriptor Descriptor { get; }
+            = OpenIddictValidationHandlerDescriptor.CreateBuilder<TContext>()
+                .AddFilter<RequireOwinRequest>()
+                .UseSingletonHandler<AttachOwinResponseChallenge<TContext>>()
+                .SetOrder(AttachHttpResponseCode<TContext>.Descriptor.Order + 1_000)
+                .SetType(OpenIddictValidationHandlerType.BuiltIn)
+                .Build();
+
+        /// <inheritdoc/>
+        public ValueTask HandleAsync(TContext context)
+        {
+            if (context is null)
+            {
+                throw new ArgumentNullException(nameof(context));
+            }
+
+            // This handler only applies to OWIN requests. If The OWIN request cannot be resolved,
+            // this may indicate that the request was incorrectly processed by another server stack.
+            var response = context.Transaction.GetOwinRequest()?.Context.Response ??
+                throw new InvalidOperationException(SR.GetResourceString(SR.ID0120));
+
+            // OWIN authentication middleware configured to use active authentication (which is the default mode)
+            // are known to aggressively intercept 401 responses even if the request is already considered fully
+            // handled. In practice, this behavior is often seen with the cookies authentication middleware,
+            // that will rewrite the 401 responses returned by OpenIddict and try to redirect the user agent
+            // to the login page configured in the options. To prevent this undesirable behavior, a fake
+            // response challenge pointing to a non-existent middleware is manually added to the OWIN context
+            // to prevent the active authentication middleware from rewriting OpenIddict's 401 HTTP responses.
+            //
+            // Note: while 403 responses are generally not intercepted by the built-in OWIN authentication
+            // middleware, they are treated the same way as 401 responses to account for custom middleware
+            // that may potentially use the same interception logic for both 401 and 403 HTTP responses.
+            if (response.StatusCode is 401 or 403 &&
+                response.Context.Authentication.AuthenticationResponseChallenge is null)
+            {
+                response.Context.Authentication.AuthenticationResponseChallenge =
+                    new AuthenticationResponseChallenge(new[] { Guid.NewGuid().ToString() }, null);
+            }
+
+            return default;
+        }
+    }
+
     /// <summary>
     /// Contains the logic responsible for attaching the appropriate HTTP response cache headers.
     /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
@@ -395,7 +437,7 @@ public static partial class OpenIddictValidationOwinHandlers
             = OpenIddictValidationHandlerDescriptor.CreateBuilder<TContext>()
                 .AddFilter<RequireOwinRequest>()
                 .UseSingletonHandler<AttachCacheControlHeader<TContext>>()
-                .SetOrder(AttachHttpResponseCode<TContext>.Descriptor.Order + 1_000)
+                .SetOrder(AttachOwinResponseChallenge<TContext>.Descriptor.Order + 1_000)
                 .SetType(OpenIddictValidationHandlerType.BuiltIn)
                 .Build();
 
@@ -463,37 +505,29 @@ public static partial class OpenIddictValidationOwinHandlers
                 return default;
             }
 
-            var scheme = context.Transaction.Response.Error switch
-            {
-                Errors.InvalidToken or
-                Errors.MissingToken or
-                Errors.InsufficientAccess or
-                Errors.InsufficientScope => Schemes.Bearer,
-
-                _ => null
-            };
-
-            if (string.IsNullOrEmpty(scheme))
-            {
-                return default;
-            }
+            // Note: unlike the server stack, the validation stack doesn't expose any endpoint
+            // and thus never returns responses containing a formatted body (e.g a JSON response).
+            //
+            // As such, all errors - even errors indicating an invalid request - are returned
+            // as part of the standard WWW-Authenticate header, as defined by the specification.
+            // See https://datatracker.ietf.org/doc/html/rfc6750#section-3 for more information.
 
             var parameters = new Dictionary<string, string>(StringComparer.Ordinal);
 
             // If a realm was configured in the options, attach it to the parameters.
-            if (!string.IsNullOrEmpty(_options.CurrentValue.Realm))
+            if (_options.CurrentValue.Realm is string { Length: > 0 } realm)
             {
-                parameters[Parameters.Realm] = _options.CurrentValue.Realm;
+                parameters[Parameters.Realm] = realm;
             }
 
             foreach (var parameter in context.Transaction.Response.GetParameters())
             {
                 // Note: the error details are only included if the error was not caused by a missing token, as recommended
                 // by the OAuth 2.0 bearer specification: https://tools.ietf.org/html/rfc6750#section-3.1.
-                if (string.Equals(context.Transaction.Response.Error, Errors.MissingToken, StringComparison.Ordinal) &&
-                   (string.Equals(parameter.Key, Parameters.Error, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorDescription, StringComparison.Ordinal) ||
-                    string.Equals(parameter.Key, Parameters.ErrorUri, StringComparison.Ordinal)))
+                if (context.Transaction.Response.Error is Errors.MissingToken &&
+                    parameter.Key is Parameters.Error            or
+                                     Parameters.ErrorDescription or
+                                     Parameters.ErrorUri)
                 {
                     continue;
                 }
@@ -508,7 +542,7 @@ public static partial class OpenIddictValidationOwinHandlers
                 parameters[parameter.Key] = value;
             }
 
-            var builder = new StringBuilder(scheme);
+            var builder = new StringBuilder(Schemes.Bearer);
 
             foreach (var parameter in parameters)
             {
@@ -575,58 +609,4 @@ public static partial class OpenIddictValidationOwinHandlers
             return default;
         }
     }
-
-    /// <summary>
-    /// Contains the logic responsible for processing OpenID Connect responses that must be returned as JSON.
-    /// Note: this handler is not used when the OpenID Connect request is not initially handled by OWIN.
-    /// </summary>
-    public class ProcessJsonResponse<TContext> : IOpenIddictValidationHandler<TContext> where TContext : BaseRequestContext
-    {
-        /// <summary>
-        /// Gets the default descriptor definition assigned to this handler.
-        /// </summary>
-        public static OpenIddictValidationHandlerDescriptor Descriptor { get; }
-            = OpenIddictValidationHandlerDescriptor.CreateBuilder<TContext>()
-                .AddFilter<RequireOwinRequest>()
-                .UseSingletonHandler<ProcessJsonResponse<TContext>>()
-                .SetOrder(ProcessChallengeErrorResponse<TContext>.Descriptor.Order + 1_000)
-                .SetType(OpenIddictValidationHandlerType.BuiltIn)
-                .Build();
-
-        /// <inheritdoc/>
-        public async ValueTask HandleAsync(TContext context)
-        {
-            if (context is null)
-            {
-                throw new ArgumentNullException(nameof(context));
-            }
-
-            Debug.Assert(context.Transaction.Response is not null, SR.GetResourceString(SR.ID4007));
-
-            // This handler only applies to OWIN requests. If The OWIN request cannot be resolved,
-            // this may indicate that the request was incorrectly processed by another server stack.
-            var response = context.Transaction.GetOwinRequest()?.Context.Response ??
-                throw new InvalidOperationException(SR.GetResourceString(SR.ID0120));
-
-            context.Logger.LogInformation(SR.GetResourceString(SR.ID6142), context.Transaction.Response);
-
-            using var stream = new MemoryStream();
-            using var writer = new Utf8JsonWriter(stream, new JsonWriterOptions
-            {
-                Encoder = JavaScriptEncoder.UnsafeRelaxedJsonEscaping,
-                Indented = true
-            });
-
-            context.Transaction.Response.WriteTo(writer);
-            writer.Flush();
-
-            response.ContentLength = stream.Length;
-            response.ContentType = "application/json;charset=UTF-8";
-
-            stream.Seek(offset: 0, loc: SeekOrigin.Begin);
-            await stream.CopyToAsync(response.Body, 4096, response.Context.Request.CallCancelled);
-
-            context.HandleRequest();
-        }
-    }
 }
diff --git a/src/OpenIddict.Validation/OpenIddictValidationHandlers.cs b/src/OpenIddict.Validation/OpenIddictValidationHandlers.cs
index 6662d0da..d959443b 100644
--- a/src/OpenIddict.Validation/OpenIddictValidationHandlers.cs
+++ b/src/OpenIddict.Validation/OpenIddictValidationHandlers.cs
@@ -24,7 +24,8 @@ public static partial class OpenIddictValidationHandlers
         /*
          * Challenge processing:
          */
-        AttachDefaultChallengeError.Descriptor)
+        AttachDefaultChallengeError.Descriptor,
+        AttachChallengeParameters.Descriptor)
 
         .AddRange(Discovery.DefaultHandlers)
         .AddRange(Introspection.DefaultHandlers)
@@ -95,11 +96,7 @@ public static partial class OpenIddictValidationHandlers
             {
                 // The validation handler is responsible for validating access tokens for endpoints
                 // it doesn't manage (typically, API endpoints using token authentication).
-                //
-                // As such, sending an access token is not mandatory: API endpoints that require
-                // authentication can set up an authorization policy to reject such requests later
-                // in the request processing pipeline (typically, via the authorization middleware).
-                OpenIddictValidationEndpointType.Unknown => (true, false, true),
+                OpenIddictValidationEndpointType.Unknown => (true, true, true),
 
                 _ => (false, false, false)
             };
@@ -123,7 +120,7 @@ public static partial class OpenIddictValidationHandlers
         /// </summary>
         public static OpenIddictValidationHandlerDescriptor Descriptor { get; }
             = OpenIddictValidationHandlerDescriptor.CreateBuilder<ProcessAuthenticationContext>()
-                .UseSingletonHandler<EvaluateValidatedTokens>()
+                .UseSingletonHandler<ValidateRequiredTokens>()
                 .SetOrder(EvaluateValidatedTokens.Descriptor.Order + 1_000)
                 .SetType(OpenIddictValidationHandlerType.BuiltIn)
                 .Build();
@@ -240,14 +237,6 @@ public static partial class OpenIddictValidationHandlers
                 throw new ArgumentNullException(nameof(context));
             }
 
-            // If an error was explicitly set by the application, don't override it.
-            if (!string.IsNullOrEmpty(context.Response.Error) ||
-                !string.IsNullOrEmpty(context.Response.ErrorDescription) ||
-                !string.IsNullOrEmpty(context.Response.ErrorUri))
-            {
-                return default;
-            }
-
             // Try to retrieve the authentication context from the validation transaction and use
             // the error details returned during the authentication processing, if available.
             // If no error is attached to the authentication context, this likely means that
@@ -258,18 +247,43 @@ public static partial class OpenIddictValidationHandlers
             var notification = context.Transaction.GetProperty<ProcessAuthenticationContext>(
                 typeof(ProcessAuthenticationContext).FullName!);
 
-            if (!string.IsNullOrEmpty(notification?.Error))
+            context.Response.Error ??= notification?.Error ?? Errors.InsufficientAccess;
+            context.Response.ErrorDescription ??= notification?.ErrorDescription ?? SR.GetResourceString(SR.ID2095);
+            context.Response.ErrorUri ??= notification?.ErrorUri ?? SR.FormatID8000(SR.ID2095);
+
+            return default;
+        }
+    }
+
+    /// <summary>
+    /// Contains the logic responsible for attaching the appropriate parameters to the challenge response.
+    /// </summary>
+    public class AttachChallengeParameters : IOpenIddictValidationHandler<ProcessChallengeContext>
+    {
+        /// <summary>
+        /// Gets the default descriptor definition assigned to this handler.
+        /// </summary>
+        public static OpenIddictValidationHandlerDescriptor Descriptor { get; }
+            = OpenIddictValidationHandlerDescriptor.CreateBuilder<ProcessChallengeContext>()
+                .UseSingletonHandler<AttachChallengeParameters>()
+                .SetOrder(AttachDefaultChallengeError.Descriptor.Order + 1_000)
+                .SetType(OpenIddictValidationHandlerType.BuiltIn)
+                .Build();
+
+        /// <inheritdoc/>
+        public ValueTask HandleAsync(ProcessChallengeContext context)
+        {
+            if (context is null)
             {
-                context.Response.Error = notification.Error;
-                context.Response.ErrorDescription = notification.ErrorDescription;
-                context.Response.ErrorUri = notification.ErrorUri;
+                throw new ArgumentNullException(nameof(context));
             }
 
-            else
+            if (context.Parameters.Count > 0)
             {
-                context.Response.Error = Errors.InsufficientAccess;
-                context.Response.ErrorDescription = SR.GetResourceString(SR.ID2095);
-                context.Response.ErrorUri = SR.FormatID8000(SR.ID2095);
+                foreach (var parameter in context.Parameters)
+                {
+                    context.Response.SetParameter(parameter.Key, parameter.Value);
+                }
             }
 
             return default;