diff --git a/src/OpenIddict.Abstractions/OpenIddictConstants.cs b/src/OpenIddict.Abstractions/OpenIddictConstants.cs
index 08fa8207..b64994f9 100644
--- a/src/OpenIddict.Abstractions/OpenIddictConstants.cs
+++ b/src/OpenIddict.Abstractions/OpenIddictConstants.cs
@@ -69,7 +69,6 @@ namespace OpenIddict.Abstractions
             public const string PreferredUsername = "preferred_username";
             public const string Profile = "profile";
             public const string Region = "region";
-            public const string Resource = "resource";
             public const string Role = "role";
             public const string Scope = "scope";
             public const string StreetAddress = "street_address";
@@ -97,6 +96,7 @@ namespace OpenIddict.Abstractions
                 public const string Nonce = "oi_nce";
                 public const string RedirectUri = "oi_reduri";
                 public const string RefreshTokenLifetime = "oi_reft_lft";
+                public const string Resource = "oi_rsrc";
                 public const string TokenUsage = "oi_tkn_use";
             }
         }
diff --git a/src/OpenIddict.Abstractions/Primitives/OpenIddictExtensions.cs b/src/OpenIddict.Abstractions/Primitives/OpenIddictExtensions.cs
index 1a9e6261..f53c040d 100644
--- a/src/OpenIddict.Abstractions/Primitives/OpenIddictExtensions.cs
+++ b/src/OpenIddict.Abstractions/Primitives/OpenIddictExtensions.cs
@@ -1110,7 +1110,7 @@ namespace OpenIddict.Abstractions
                 throw new ArgumentNullException(nameof(principal));
             }
 
-            return ImmutableHashSet.CreateRange(StringComparer.Ordinal, principal.GetClaims(Claims.Resource));
+            return ImmutableHashSet.CreateRange(StringComparer.Ordinal, principal.GetClaims(Claims.Private.Resource));
         }
 
         /// <summary>
@@ -1423,7 +1423,7 @@ namespace OpenIddict.Abstractions
                 throw new ArgumentNullException(nameof(principal));
             }
 
-            return principal.FindAll(Claims.Resource).Any();
+            return principal.FindAll(Claims.Private.Resource).Any();
         }
 
         /// <summary>
@@ -1611,7 +1611,7 @@ namespace OpenIddict.Abstractions
                 throw new ArgumentNullException(nameof(principal));
             }
 
-            return principal.SetClaims(Claims.Resource, resources.Distinct(StringComparer.Ordinal));
+            return principal.SetClaims(Claims.Private.Resource, resources.Distinct(StringComparer.Ordinal));
         }
 
         /// <summary>
diff --git a/src/OpenIddict.Server/OpenIddictServerHandlers.cs b/src/OpenIddict.Server/OpenIddictServerHandlers.cs
index a66120b8..fabd75b0 100644
--- a/src/OpenIddict.Server/OpenIddictServerHandlers.cs
+++ b/src/OpenIddict.Server/OpenIddictServerHandlers.cs
@@ -43,6 +43,7 @@ namespace OpenIddict.Server
             ValidateSigninResponse.Descriptor,
             AttachDefaultScopes.Descriptor,
             AttachDefaultPresenters.Descriptor,
+            InferResources.Descriptor,
             EvaluateReturnedTokens.Descriptor,
             AttachAccessToken.Descriptor,
             AttachAuthorizationCode.Descriptor,
@@ -300,6 +301,47 @@ namespace OpenIddict.Server
             }
         }
 
+        /// <summary>
+        /// Contains the logic responsible of inferring resources from the audience claims if necessary.
+        /// </summary>
+        public class InferResources : IOpenIddictServerHandler<ProcessSigninContext>
+        {
+            /// <summary>
+            /// Gets the default descriptor definition assigned to this handler.
+            /// </summary>
+            public static OpenIddictServerHandlerDescriptor Descriptor { get; }
+                = OpenIddictServerHandlerDescriptor.CreateBuilder<ProcessSigninContext>()
+                    .UseSingletonHandler<InferResources>()
+                    .SetOrder(AttachDefaultPresenters.Descriptor.Order + 1_000)
+                    .Build();
+
+            /// <summary>
+            /// Processes the event.
+            /// </summary>
+            /// <param name="context">The context associated with the event to process.</param>
+            /// <returns>
+            /// A <see cref="ValueTask"/> that can be used to monitor the asynchronous operation.
+            /// </returns>
+            public ValueTask HandleAsync([NotNull] ProcessSigninContext context)
+            {
+                if (context == null)
+                {
+                    throw new ArgumentNullException(nameof(context));
+                }
+
+                // When a "resources" property cannot be found in the ticket, infer it from the "audiences" property.
+                if (context.Principal.HasAudience() && !context.Principal.HasResource())
+                {
+                    context.Principal.SetResources(context.Principal.GetAudiences());
+                }
+
+                // Reset the audiences collection, as it's later set, based on the token type.
+                context.Principal.SetAudiences(Array.Empty<string>());
+
+                return default;
+            }
+        }
+
         /// <summary>
         /// Contains the logic responsible of selecting the token types returned to the client application.
         /// </summary>
@@ -311,7 +353,7 @@ namespace OpenIddict.Server
             public static OpenIddictServerHandlerDescriptor Descriptor { get; }
                 = OpenIddictServerHandlerDescriptor.CreateBuilder<ProcessSigninContext>()
                     .UseSingletonHandler<EvaluateReturnedTokens>()
-                    .SetOrder(AttachDefaultPresenters.Descriptor.Order + 1_000)
+                    .SetOrder(InferResources.Descriptor.Order + 1_000)
                     .Build();
 
             /// <summary>
@@ -448,6 +490,12 @@ namespace OpenIddict.Server
                     return true;
                 });
 
+                // Remove the destinations from the claim properties.
+                foreach (var claim in principal.Claims)
+                {
+                    claim.Properties.Remove(OpenIddictConstants.Properties.Destinations);
+                }
+
                 principal.SetTokenId(Guid.NewGuid().ToString()).SetCreationDate(DateTimeOffset.UtcNow);
 
                 var lifetime = context.Principal.GetAccessTokenLifetime() ?? context.Options.AccessTokenLifetime;
@@ -456,11 +504,8 @@ namespace OpenIddict.Server
                     principal.SetExpirationDate(principal.GetCreationDate() + lifetime.Value);
                 }
 
-                // Remove the destinations from the claim properties.
-                foreach (var claim in principal.Claims)
-                {
-                    claim.Properties.Remove(OpenIddictConstants.Properties.Destinations);
-                }
+                // Set the audiences collection using the private resource claims stored in the principal.
+                principal.SetAudiences(context.Principal.GetResources());
 
                 // When receiving a grant_type=refresh_token request, determine whether the client application
                 // requests a limited set of scopes and immediately replace the scopes collection if necessary.
@@ -702,14 +747,14 @@ namespace OpenIddict.Server
                     return true;
                 });
 
-                principal.SetTokenId(Guid.NewGuid().ToString()).SetCreationDate(DateTimeOffset.UtcNow);
-
                 // Remove the destinations from the claim properties.
                 foreach (var claim in principal.Claims)
                 {
                     claim.Properties.Remove(OpenIddictConstants.Properties.Destinations);
                 }
 
+                principal.SetTokenId(Guid.NewGuid().ToString()).SetCreationDate(DateTimeOffset.UtcNow);
+
                 var lifetime = context.Principal.GetIdentityTokenLifetime() ?? context.Options.IdentityTokenLifetime;
                 if (lifetime.HasValue)
                 {