diff --git a/src/Headless/Avalonia.Headless/HeadlessUnitTestSession.cs b/src/Headless/Avalonia.Headless/HeadlessUnitTestSession.cs
index 5613244461..f215d867f0 100644
--- a/src/Headless/Avalonia.Headless/HeadlessUnitTestSession.cs
+++ b/src/Headless/Avalonia.Headless/HeadlessUnitTestSession.cs
@@ -145,7 +145,16 @@ public sealed class HeadlessUnitTestSession : IDisposable, IAsyncDisposable
             }
             finally
             {
-                application.Dispose();
+                try
+                {
+                    application.Dispose();
+                }
+                catch (Exception ex)
+                {
+                    // Cleanup runs before the TCS is completed, so its failure must be
+                    // reported by this work item instead of escaping the consumer loop.
+                    caught = ex;
+                }
             }
 
             if (caught != null)
@@ -173,8 +182,14 @@ public sealed class HeadlessUnitTestSession : IDisposable, IAsyncDisposable
 
         return Disposable.Create(() =>
         {
-            Dispatcher.UIThread.RunJobs();
-            SynchronizationContext.SetSynchronizationContext(oldContext);
+            try
+            {
+                Dispatcher.UIThread.RunJobs();
+            }
+            finally
+            {
+                SynchronizationContext.SetSynchronizationContext(oldContext);
+            }
         });
     }
 
@@ -195,12 +210,25 @@ public sealed class HeadlessUnitTestSession : IDisposable, IAsyncDisposable
 
         return Disposable.Create(() =>
         {
-            ((ToolTipService?)AvaloniaLocator.Current.GetService<IToolTipService>())?.Dispose();
-            (AvaloniaLocator.Current.GetService<FontManager>() as IDisposable)?.Dispose();
-            Dispatcher.ResetForUnitTests();
-            scope.Dispose();
-            Dispatcher.ResetBeforeUnitTests();
-            SynchronizationContext.SetSynchronizationContext(oldContext);
+            try
+            {
+                ((ToolTipService?)AvaloniaLocator.Current.GetService<IToolTipService>())?.Dispose();
+                (AvaloniaLocator.Current.GetService<FontManager>() as IDisposable)?.Dispose();
+                Dispatcher.ResetForUnitTests();
+            }
+            finally
+            {
+                // Cleanup jobs can throw, but the ambient state still belongs to this dispatch.
+                try
+                {
+                    scope.Dispose();
+                }
+                finally
+                {
+                    Dispatcher.ResetBeforeUnitTests();
+                    SynchronizationContext.SetSynchronizationContext(oldContext);
+                }
+            }
         });
     }
 
diff --git a/tests/Avalonia.Headless.UnitTests/HeadlessUnitTestSessionTests.cs b/tests/Avalonia.Headless.UnitTests/HeadlessUnitTestSessionTests.cs
new file mode 100644
index 0000000000..7372dd639a
--- /dev/null
+++ b/tests/Avalonia.Headless.UnitTests/HeadlessUnitTestSessionTests.cs
@@ -0,0 +1,32 @@
+#if NUNIT
+using System;
+using System.Threading;
+using System.Threading.Tasks;
+using Avalonia.Threading;
+
+namespace Avalonia.Headless.UnitTests;
+
+public class HeadlessUnitTestSessionTests
+{
+    [Test]
+    public async Task Dispatch_Should_Report_Cleanup_Exceptions_And_Continue()
+    {
+        var session = HeadlessUnitTestSession.GetOrStartForAssembly(GetType().Assembly);
+
+        const string message = "Thrown by a dispatcher job during cleanup.";
+        var poisonedDispatch = session.Dispatch(
+            () => Dispatcher.UIThread.Post(() => throw new InvalidOperationException(message)),
+            CancellationToken.None);
+
+        var exception = Assert.ThrowsAsync<InvalidOperationException>(async () =>
+            await poisonedDispatch.WaitAsync(TimeSpan.FromSeconds(10)));
+
+        Assert.That(exception!.Message, Is.EqualTo(message));
+
+        var result = await session.Dispatch(() => 42, CancellationToken.None)
+            .WaitAsync(TimeSpan.FromSeconds(10));
+
+        Assert.That(result, Is.EqualTo(42));
+    }
+}
+#endif