diff --git a/src/Microsoft.AspNetCore.Server.HttpSys/MessagePump.cs b/src/Microsoft.AspNetCore.Server.HttpSys/MessagePump.cs
index 82e6a03039..53330c6f1c 100644
--- a/src/Microsoft.AspNetCore.Server.HttpSys/MessagePump.cs
+++ b/src/Microsoft.AspNetCore.Server.HttpSys/MessagePump.cs
@@ -25,9 +25,10 @@ namespace Microsoft.AspNetCore.Server.HttpSys
         private int _acceptorCounts;
         private Action<object> _processRequest;
 
-        private bool _stopping;
+        private volatile int _stopping;
         private int _outstandingRequests;
-        private TaskCompletionSource<object> _shutdownSignal;
+        private readonly TaskCompletionSource<object> _shutdownSignal = new TaskCompletionSource<object>(TaskCreationOptions.RunContinuationsAsynchronously);
+        private int _shutdownSignalCompleted;
 
         private readonly ServerAddressesFeature _serverAddresses;
 
@@ -56,13 +57,14 @@ namespace Microsoft.AspNetCore.Server.HttpSys
 
             _processRequest = new Action<object>(ProcessRequestAsync);
             _maxAccepts = _options.MaxAccepts;
-            _shutdownSignal = new TaskCompletionSource<object>();
         }
 
         internal HttpSysListener Listener { get; }
 
         public IFeatureCollection Features { get; }
 
+        private bool Stopping => _stopping == 1;
+
         public Task StartAsync<TContext>(IHttpApplication<TContext> application, CancellationToken cancellationToken)
         {
             if (application == null)
@@ -146,7 +148,7 @@ namespace Microsoft.AspNetCore.Server.HttpSys
         private async void ProcessRequestsWorker()
         {
             int workerIndex = Interlocked.Increment(ref _acceptorCounts);
-            while (!_stopping && workerIndex <= _maxAccepts)
+            while (!Stopping && workerIndex <= _maxAccepts)
             {
                 // Receive a request
                 RequestContext requestContext;
@@ -156,8 +158,8 @@ namespace Microsoft.AspNetCore.Server.HttpSys
                 }
                 catch (Exception exception)
                 {
-                    Contract.Assert(_stopping);
-                    if (_stopping)
+                    Contract.Assert(Stopping);
+                    if (Stopping)
                     {
                         LogHelper.LogDebug(_logger, "ListenForNextRequestAsync-Stopping", exception);
                     }
@@ -186,7 +188,7 @@ namespace Microsoft.AspNetCore.Server.HttpSys
             var requestContext = requestContextObj as RequestContext;
             try
             {
-                if (_stopping)
+                if (Stopping)
                 {
                     SetFatalResponse(requestContext, 503);
                     return;
@@ -227,7 +229,7 @@ namespace Microsoft.AspNetCore.Server.HttpSys
                 }
                 finally
                 {
-                    if (Interlocked.Decrement(ref _outstandingRequests) == 0 && _stopping)
+                    if (Interlocked.Decrement(ref _outstandingRequests) == 0 && Stopping)
                     {
                         LogHelper.LogInfo(_logger, "All requests drained.");
                         _shutdownSignal.TrySetResult(0);
@@ -250,28 +252,51 @@ namespace Microsoft.AspNetCore.Server.HttpSys
 
         public Task StopAsync(CancellationToken cancellationToken)
         {
-            _stopping = true;
-            // Wait for active requests to drain
-            if (_outstandingRequests > 0)
+            void RegisterCancelation()
             {
-                LogHelper.LogInfo(_logger, "Stopping, waiting for " + _outstandingRequests + " request(s) to drain.");
-
-                var waitForStop = new TaskCompletionSource<object>();
                 cancellationToken.Register(() =>
                 {
-                    LogHelper.LogInfo(_logger, "Timed out, terminating " + _outstandingRequests + " request(s).");
-                    waitForStop.TrySetResult(0);
+                    if (Interlocked.Exchange(ref _shutdownSignalCompleted, 1) == 0)
+                    {
+                        LogHelper.LogInfo(_logger, "Canceled, terminating " + _outstandingRequests + " request(s).");
+                        _shutdownSignal.TrySetResult(null);
+                    }
                 });
-
-                return Task.WhenAny(_shutdownSignal.Task, waitForStop.Task);
             }
 
-            return Task.CompletedTask;
+            if (Interlocked.Exchange(ref _stopping, 1) == 1)
+            {
+                RegisterCancelation();
+
+                return _shutdownSignal.Task;
+            }
+
+            try
+            {
+                // Wait for active requests to drain
+                if (_outstandingRequests > 0)
+                {
+                    LogHelper.LogInfo(_logger, "Stopping, waiting for " + _outstandingRequests + " request(s) to drain.");
+                    RegisterCancelation();
+                }
+                else
+                {
+                    _shutdownSignal.TrySetResult(null);
+                }
+            }
+            catch (Exception ex)
+            {
+                _shutdownSignal.TrySetException(ex);
+            }
+
+            return _shutdownSignal.Task;
         }
 
         public void Dispose()
         {
-            _stopping = true;
+            _stopping = 1;
+            _shutdownSignal.TrySetResult(null);
+
             Listener.Dispose();
         }
 
diff --git a/test/Microsoft.AspNetCore.Server.HttpSys.FunctionalTests/ServerTests.cs b/test/Microsoft.AspNetCore.Server.HttpSys.FunctionalTests/ServerTests.cs
index 9e5bc9e444..b5c9734bb7 100644
--- a/test/Microsoft.AspNetCore.Server.HttpSys.FunctionalTests/ServerTests.cs
+++ b/test/Microsoft.AspNetCore.Server.HttpSys.FunctionalTests/ServerTests.cs
@@ -11,6 +11,7 @@ using System.Threading;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.Authentication;
 using Microsoft.AspNetCore.Http;
+using Microsoft.AspNetCore.Testing;
 using Microsoft.AspNetCore.Testing.xunit;
 using Microsoft.Extensions.Logging;
 using Microsoft.Extensions.Options;
@@ -406,6 +407,194 @@ namespace Microsoft.AspNetCore.Server.HttpSys
             }
         }
 
+        [ConditionalFact]
+        public async Task Server_MultipleStopAsyncCallsWaitForRequestsToDrain_Success()
+        {
+            Task<string> responseTask;
+            ManualResetEvent received = new ManualResetEvent(false);
+            ManualResetEvent run = new ManualResetEvent(false);
+            string address;
+            using (var server = Utilities.CreateHttpServer(out address, httpContext =>
+                {
+                    received.Set();
+                    Assert.True(run.WaitOne(TimeSpan.FromSeconds(10)));
+                    httpContext.Response.ContentLength = 11;
+                    return httpContext.Response.WriteAsync("Hello World");
+                }))
+            {
+                responseTask = SendRequestAsync(address);
+                Assert.True(received.WaitOne(TimeSpan.FromSeconds(10)));
+
+                var cts = new CancellationTokenSource(TimeSpan.FromSeconds(10));
+                var stopTask1 = server.StopAsync(cts.Token);
+                var stopTask2 = server.StopAsync(cts.Token);
+                var stopTask3 = server.StopAsync(cts.Token);
+
+                Assert.False(stopTask1.IsCompleted);
+                Assert.False(stopTask2.IsCompleted);
+                Assert.False(stopTask3.IsCompleted);
+
+                run.Set();
+
+                await Task.WhenAll(stopTask1, stopTask2, stopTask3).TimeoutAfter(TimeSpan.FromSeconds(10));
+            }
+            string response = await responseTask;
+            Assert.Equal("Hello World", response);
+        }
+
+        [ConditionalFact]
+        public async Task Server_MultipleStopAsyncCallsCompleteOnCancellation_SameToken_Success()
+        {
+            Task<string> responseTask;
+            ManualResetEvent received = new ManualResetEvent(false);
+            ManualResetEvent run = new ManualResetEvent(false);
+            string address;
+            using (var server = Utilities.CreateHttpServer(out address, httpContext =>
+                {
+                    received.Set();
+                    Assert.True(run.WaitOne(TimeSpan.FromSeconds(10)));
+                    httpContext.Response.ContentLength = 11;
+                    return httpContext.Response.WriteAsync("Hello World");
+                }))
+            {
+                responseTask = SendRequestAsync(address);
+                Assert.True(received.WaitOne(TimeSpan.FromSeconds(10)));
+
+                var cts = new CancellationTokenSource();
+                var stopTask1 = server.StopAsync(cts.Token);
+                var stopTask2 = server.StopAsync(cts.Token);
+                var stopTask3 = server.StopAsync(cts.Token);
+
+                Assert.False(stopTask1.IsCompleted);
+                Assert.False(stopTask2.IsCompleted);
+                Assert.False(stopTask3.IsCompleted);
+
+                cts.Cancel();
+
+                await Task.WhenAll(stopTask1, stopTask2, stopTask3).TimeoutAfter(TimeSpan.FromSeconds(10));
+
+                run.Set();
+
+                string response = await responseTask;
+                Assert.Equal("Hello World", response);
+            }
+        }
+
+        [ConditionalFact]
+        public async Task Server_MultipleStopAsyncCallsCompleteOnSingleCancellation_FirstToken_Success()
+        {
+            Task<string> responseTask;
+            ManualResetEvent received = new ManualResetEvent(false);
+            ManualResetEvent run = new ManualResetEvent(false);
+            string address;
+            using (var server = Utilities.CreateHttpServer(out address, httpContext =>
+                {
+                    received.Set();
+                    Assert.True(run.WaitOne(TimeSpan.FromSeconds(10)));
+                    httpContext.Response.ContentLength = 11;
+                    return httpContext.Response.WriteAsync("Hello World");
+                }))
+            {
+                responseTask = SendRequestAsync(address);
+                Assert.True(received.WaitOne(TimeSpan.FromSeconds(10)));
+
+                var cts = new CancellationTokenSource();
+                var stopTask1 = server.StopAsync(cts.Token);
+                var stopTask2 = server.StopAsync(new CancellationTokenSource().Token);
+                var stopTask3 = server.StopAsync(new CancellationTokenSource().Token);
+
+                Assert.False(stopTask1.IsCompleted);
+                Assert.False(stopTask2.IsCompleted);
+                Assert.False(stopTask3.IsCompleted);
+
+                cts.Cancel();
+
+                await Task.WhenAll(stopTask1, stopTask2, stopTask3).TimeoutAfter(TimeSpan.FromSeconds(10));
+
+                run.Set();
+
+                string response = await responseTask;
+                Assert.Equal("Hello World", response);
+            }
+        }
+
+        [ConditionalFact]
+        public async Task Server_MultipleStopAsyncCallsCompleteOnSingleCancellation_SubsequentToken_Success()
+        {
+            Task<string> responseTask;
+            ManualResetEvent received = new ManualResetEvent(false);
+            ManualResetEvent run = new ManualResetEvent(false);
+            string address;
+            using (var server = Utilities.CreateHttpServer(out address, httpContext =>
+                {
+                    received.Set();
+                    Assert.True(run.WaitOne(TimeSpan.FromSeconds(10)));
+                    httpContext.Response.ContentLength = 11;
+                    return httpContext.Response.WriteAsync("Hello World");
+                }))
+            {
+                responseTask = SendRequestAsync(address);
+                Assert.True(received.WaitOne(10000));
+
+                var cts = new CancellationTokenSource();
+                var stopTask1 = server.StopAsync(new CancellationTokenSource().Token);
+                var stopTask2 = server.StopAsync(cts.Token);
+                var stopTask3 = server.StopAsync(new CancellationTokenSource().Token);
+
+                Assert.False(stopTask1.IsCompleted);
+                Assert.False(stopTask2.IsCompleted);
+                Assert.False(stopTask3.IsCompleted);
+
+                cts.Cancel();
+
+                await Task.WhenAll(stopTask1, stopTask2, stopTask3).TimeoutAfter(TimeSpan.FromSeconds(10));
+
+                run.Set();
+
+                string response = await responseTask;
+                Assert.Equal("Hello World", response);
+            }
+        }
+
+        [ConditionalFact]
+        public async Task Server_DisposeContinuesPendingStopAsyncCalls()
+        {
+            Task<string> responseTask;
+            ManualResetEvent received = new ManualResetEvent(false);
+            ManualResetEvent run = new ManualResetEvent(false);
+            string address;
+            Task stopTask1;
+            Task stopTask2;
+            using (var server = Utilities.CreateHttpServer(out address, httpContext =>
+                {
+                    received.Set();
+                    Assert.True(run.WaitOne(TimeSpan.FromSeconds(10)));
+                    httpContext.Response.ContentLength = 11;
+                    return httpContext.Response.WriteAsync("Hello World");
+                }))
+            {
+                responseTask = SendRequestAsync(address);
+                Assert.True(received.WaitOne(TimeSpan.FromSeconds(10)));
+
+                stopTask1 = server.StopAsync(new CancellationTokenSource().Token);
+                stopTask2 = server.StopAsync(new CancellationTokenSource().Token);
+
+                Assert.False(stopTask1.IsCompleted);
+                Assert.False(stopTask2.IsCompleted);
+            }
+
+            await Task.WhenAll(stopTask1, stopTask2).TimeoutAfter(TimeSpan.FromSeconds(10));
+        }
+
+        [ConditionalFact]
+        public async Task Server_StopAsyncCalledWithNoRequests_Success()
+        {
+            using (var server = Utilities.CreateHttpServer(out _, httpContext => Task.CompletedTask))
+            {
+                await server.StopAsync(default(CancellationToken)).TimeoutAfter(TimeSpan.FromSeconds(10));
+            }
+        }
+
         private async Task<string> SendRequestAsync(string uri)
         {
             using (HttpClient client = new HttpClient())