diff --git a/src/Hosting/TestHost/src/HttpContextBuilder.cs b/src/Hosting/TestHost/src/HttpContextBuilder.cs
index 87d408feaa70..f6e1279fc4ff 100644
--- a/src/Hosting/TestHost/src/HttpContextBuilder.cs
+++ b/src/Hosting/TestHost/src/HttpContextBuilder.cs
@@ -83,7 +83,14 @@ internal void RegisterResponseReadCompleteCallback(Action<HttpContext> responseR
     /// <returns></returns>
     internal Task<HttpContext> SendAsync(CancellationToken cancellationToken)
     {
-        var registration = cancellationToken.Register(ClientInitiatedAbort);
+        var registration = cancellationToken.Register(() =>
+        {
+            ClientInitiatedAbort();
+
+            // The client gave up on this request. Fail its task now, the way a real server would, instead of
+            // waiting for an application that may never check RequestAborted.
+            _responseTcs.TrySetException(new OperationCanceledException("The request was canceled.", cancellationToken));
+        });
 
         // Everything inside this function happens in the SERVER's execution context (unless PreserveExecutionContext is true)
         async Task RunRequestAsync()
diff --git a/src/Hosting/TestHost/test/TestClientTests.cs b/src/Hosting/TestHost/test/TestClientTests.cs
index 5d3d774a3e37..c3af08d2750f 100644
--- a/src/Hosting/TestHost/test/TestClientTests.cs
+++ b/src/Hosting/TestHost/test/TestClientTests.cs
@@ -1081,6 +1081,40 @@ public async Task ClientCancellationAbortsRequest()
         var exception = await Assert.ThrowsAnyAsync<OperationCanceledException>(async () => await tcs.Task);
     }
 
+    [Fact]
+    public async Task ClientCancellationThrowsWithoutWaitingForApplication()
+    {
+        var applicationStarted = new TaskCompletionSource(TaskCreationOptions.RunContinuationsAsynchronously);
+        var applicationCompleted = new TaskCompletionSource(TaskCreationOptions.RunContinuationsAsynchronously);
+
+        var builder = new HostBuilder()
+            .ConfigureWebHost(webHostBuilder =>
+            {
+                webHostBuilder
+                    .UseTestServer()
+                    .Configure(app => app.Run(async ctx =>
+                    {
+                        // The application never observes RequestAborted and keeps running after the client gives up.
+                        applicationStarted.SetResult();
+                        await applicationCompleted.Task;
+                    }));
+            });
+        using var host = builder.Build();
+        await host.StartAsync();
+
+        using var server = host.GetTestServer();
+        using var client = server.CreateClient();
+        using var cts = new CancellationTokenSource();
+
+        var requestTask = client.GetAsync("http://localhost:12345", cts.Token);
+        await applicationStarted.Task.DefaultTimeout();
+        cts.Cancel();
+
+        await Assert.ThrowsAnyAsync<OperationCanceledException>(() => requestTask.DefaultTimeout());
+
+        applicationCompleted.SetResult();
+    }
+
     [Fact]
     public async Task AsyncLocalValueOnClientIsNotPreserved()
     {