diff --git a/src/Microsoft.AspNetCore.TestHost/ClientHandler.cs b/src/Microsoft.AspNetCore.TestHost/ClientHandler.cs
index af01a88619..87454d7530 100644
--- a/src/Microsoft.AspNetCore.TestHost/ClientHandler.cs
+++ b/src/Microsoft.AspNetCore.TestHost/ClientHandler.cs
@@ -81,7 +81,7 @@ namespace Microsoft.AspNetCore.TestHost
                     try
                     {
                         await _application.ProcessRequestAsync(state.Context);
-                        state.CompleteResponse();
+                        await state.CompleteResponseAsync();
                         state.ServerCleanup(exception: null);
                     }
                     catch (Exception ex)
@@ -165,7 +165,7 @@ namespace Microsoft.AspNetCore.TestHost
                     }
                 }
 
-                _responseStream = new ResponseStream(ReturnResponseMessage, AbortRequest);
+                _responseStream = new ResponseStream(ReturnResponseMessageAsync, AbortRequest);
                 httpContext.Response.Body = _responseStream;
                 httpContext.Response.StatusCode = 200;
                 httpContext.RequestAborted = _requestAbortedSource.Token;
@@ -187,27 +187,30 @@ namespace Microsoft.AspNetCore.TestHost
                 _responseStream.Complete();
             }
 
-            internal void CompleteResponse()
+            internal async Task CompleteResponseAsync()
             {
                 _pipelineFinished = true;
-                ReturnResponseMessage();
+                await ReturnResponseMessageAsync();
                 _responseStream.Complete();
-                _responseFeature.FireOnResponseCompleted();
+                await _responseFeature.FireOnResponseCompletedAsync();
             }
 
-            internal void ReturnResponseMessage()
+            internal async Task ReturnResponseMessageAsync()
             {
-                if (!_responseTcs.Task.IsCompleted)
+                // Check if the response has already started because the TrySetResult below could happen a bit late
+                // (as it happens on a different thread) by which point the CompleteResponseAsync could run and calls this
+                // method again.
+                if (!Context.HttpContext.Response.HasStarted)
                 {
-                    var response = GenerateResponse();
+                    var response = await GenerateResponseAsync();
                     // Dispatch, as TrySetResult will synchronously execute the waiters callback and block our Write.
-                    Task.Factory.StartNew(() => _responseTcs.TrySetResult(response));
+                    var setResult = Task.Factory.StartNew(() => _responseTcs.TrySetResult(response));
                 }
             }
 
-            private HttpResponseMessage GenerateResponse()
+            private async Task<HttpResponseMessage> GenerateResponseAsync()
             {
-                _responseFeature.FireOnSendingHeaders();
+                await _responseFeature.FireOnSendingHeadersAsync();
                 var httpContext = Context.HttpContext;
 
                 var response = new HttpResponseMessage();
diff --git a/src/Microsoft.AspNetCore.TestHost/ResponseFeature.cs b/src/Microsoft.AspNetCore.TestHost/ResponseFeature.cs
index 873da77a21..73a17f6d33 100644
--- a/src/Microsoft.AspNetCore.TestHost/ResponseFeature.cs
+++ b/src/Microsoft.AspNetCore.TestHost/ResponseFeature.cs
@@ -11,8 +11,8 @@ namespace Microsoft.AspNetCore.TestHost
 {
     internal class ResponseFeature : IHttpResponseFeature
     {
-        private Action _responseStarting = () => { };
-        private Action _responseCompleted = () => { };
+        private Func<Task> _responseStartingAsync = () => Task.FromResult(true);
+        private Func<Task> _responseCompletedAsync = () => Task.FromResult(true);
 
         public ResponseFeature()
         {
@@ -36,33 +36,39 @@ namespace Microsoft.AspNetCore.TestHost
 
         public void OnStarting(Func<object, Task> callback, object state)
         {
-            var prior = _responseStarting;
-            _responseStarting = () =>
+            var prior = _responseStartingAsync;
+            _responseStartingAsync = async () =>
             {
-                callback(state);
-                prior();
+                await callback(state);
+                await prior();
             };
         }
 
         public void OnCompleted(Func<object, Task> callback, object state)
         {
-            var prior = _responseCompleted;
-            _responseCompleted = () =>
+            var prior = _responseCompletedAsync;
+            _responseCompletedAsync = async () =>
             {
-                callback(state);
-                prior();
+                try
+                {
+                    await callback(state);
+                }
+                finally
+                {
+                    await prior();
+                }
             };
         }
 
-        public void FireOnSendingHeaders()
+        public async Task FireOnSendingHeadersAsync()
         {
-            _responseStarting();
+            await _responseStartingAsync();
             HasStarted = true;
         }
 
-        public void FireOnResponseCompleted()
+        public Task FireOnResponseCompletedAsync()
         {
-            _responseCompleted();
+            return _responseCompletedAsync();
         }
     }
 }
diff --git a/src/Microsoft.AspNetCore.TestHost/ResponseStream.cs b/src/Microsoft.AspNetCore.TestHost/ResponseStream.cs
index 85ee89e3bb..df3a02fcfc 100644
--- a/src/Microsoft.AspNetCore.TestHost/ResponseStream.cs
+++ b/src/Microsoft.AspNetCore.TestHost/ResponseStream.cs
@@ -24,15 +24,15 @@ namespace Microsoft.AspNetCore.TestHost
         private TaskCompletionSource<object> _readWaitingForData;
         private object _signalReadLock;
 
-        private Action _onFirstWrite;
+        private Func<Task> _onFirstWriteAsync;
         private bool _firstWrite;
         private Action _abortRequest;
 
-        internal ResponseStream(Action onFirstWrite, Action abortRequest)
+        internal ResponseStream(Func<Task> onFirstWriteAsync, Action abortRequest)
         {
-            if (onFirstWrite == null)
+            if (onFirstWriteAsync == null)
             {
-                throw new ArgumentNullException(nameof(onFirstWrite));
+                throw new ArgumentNullException(nameof(onFirstWriteAsync));
             }
 
             if (abortRequest == null)
@@ -40,7 +40,7 @@ namespace Microsoft.AspNetCore.TestHost
                 throw new ArgumentNullException(nameof(abortRequest));
             }
 
-            _onFirstWrite = onFirstWrite;
+            _onFirstWriteAsync = onFirstWriteAsync;
             _firstWrite = true;
             _abortRequest = abortRequest;
 
@@ -98,7 +98,7 @@ namespace Microsoft.AspNetCore.TestHost
             _writeLock.Wait();
             try
             {
-                FirstWrite();
+                FirstWriteAsync().GetAwaiter().GetResult();
             }
             finally
             {
@@ -230,13 +230,14 @@ namespace Microsoft.AspNetCore.TestHost
         }
 
         // Called under write-lock.
-        private void FirstWrite()
+        private Task FirstWriteAsync()
         {
             if (_firstWrite)
             {
                 _firstWrite = false;
-                _onFirstWrite();
+                return _onFirstWriteAsync();
             }
+            return Task.FromResult(true);
         }
 
         // Write with count 0 will still trigger OnFirstWrite
@@ -248,7 +249,7 @@ namespace Microsoft.AspNetCore.TestHost
             _writeLock.Wait();
             try
             {
-                FirstWrite();
+                FirstWriteAsync().GetAwaiter().GetResult();
                 if (count == 0)
                 {
                     return;
diff --git a/test/Microsoft.AspNetCore.TestHost.Tests/ResponseFeatureTests.cs b/test/Microsoft.AspNetCore.TestHost.Tests/ResponseFeatureTests.cs
index dc8831fc99..9ab936bb81 100644
--- a/test/Microsoft.AspNetCore.TestHost.Tests/ResponseFeatureTests.cs
+++ b/test/Microsoft.AspNetCore.TestHost.Tests/ResponseFeatureTests.cs
@@ -1,6 +1,7 @@
 // Copyright (c) .NET Foundation. All rights reserved.
 // Licensed under the Apache License, Version 2.0. See License.txt in the project root for license information.
 
+using System.Threading.Tasks;
 using Xunit;
 
 namespace Microsoft.AspNetCore.TestHost
@@ -8,7 +9,7 @@ namespace Microsoft.AspNetCore.TestHost
     public class ResponseFeatureTests
     {
         [Fact]
-        public void StatusCode_DefaultsTo200()
+        public async Task StatusCode_DefaultsTo200()
         {
             // Arrange & Act
             var responseInformation = new ResponseFeature();
@@ -17,7 +18,7 @@ namespace Microsoft.AspNetCore.TestHost
             Assert.Equal(200, responseInformation.StatusCode);
             Assert.False(responseInformation.HasStarted);
 
-            responseInformation.FireOnSendingHeaders();
+            await responseInformation.FireOnSendingHeadersAsync();
 
             Assert.True(responseInformation.HasStarted);
         }