diff --git a/src/Microsoft.Net.Http.Server/RequestProcessing/RequestContext.cs b/src/Microsoft.Net.Http.Server/RequestProcessing/RequestContext.cs
index 5ad6bbf78d..34b68d7242 100644
--- a/src/Microsoft.Net.Http.Server/RequestProcessing/RequestContext.cs
+++ b/src/Microsoft.Net.Http.Server/RequestProcessing/RequestContext.cs
@@ -69,16 +69,24 @@ namespace Microsoft.Net.Http.Server
                 // We need to be able to dispose of the registrations each request to prevent leaks.
                 if (!_disconnectToken.HasValue)
                 {
-                    var connectionDisconnectToken = Server.DisconnectListener.GetTokenForConnection(Request.UConnectionId);
-
-                    if (connectionDisconnectToken.CanBeCanceled)
+                    if (_disposed || Response.BodyIsFinished)
                     {
-                        _requestAbortSource = CancellationTokenSource.CreateLinkedTokenSource(connectionDisconnectToken);
-                        _disconnectToken = _requestAbortSource.Token;
+                        // We cannot register for disconnect notifications after the response has finished sending.
+                        _disconnectToken = CancellationToken.None;
                     }
                     else
                     {
-                        _disconnectToken = CancellationToken.None;
+                        var connectionDisconnectToken = Server.DisconnectListener.GetTokenForConnection(Request.UConnectionId);
+
+                        if (connectionDisconnectToken.CanBeCanceled)
+                        {
+                            _requestAbortSource = CancellationTokenSource.CreateLinkedTokenSource(connectionDisconnectToken);
+                            _disconnectToken = _requestAbortSource.Token;
+                        }
+                        else
+                        {
+                            _disconnectToken = CancellationToken.None;
+                        }
                     }
                 }
                 return _disconnectToken.Value;
diff --git a/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs b/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs
index 3ff9af71cd..1c6dc9c2c9 100644
--- a/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs
+++ b/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs
@@ -115,6 +115,8 @@ namespace Microsoft.Net.Http.Server
             }
         }
 
+        internal bool BodyIsFinished => _nativeStream?.IsDisposed ?? _responseState >= ResponseState.Closed;
+
         /// <summary>
         /// The authentication challenges that will be added to the response if the status code is 401.
         /// This must be a subset of the AuthenticationSchemes enabled on the server.
diff --git a/src/Microsoft.Net.Http.Server/RequestProcessing/ResponseStream.cs b/src/Microsoft.Net.Http.Server/RequestProcessing/ResponseStream.cs
index cacb354851..b5bfca3915 100644
--- a/src/Microsoft.Net.Http.Server/RequestProcessing/ResponseStream.cs
+++ b/src/Microsoft.Net.Http.Server/RequestProcessing/ResponseStream.cs
@@ -63,6 +63,8 @@ namespace Microsoft.Net.Http.Server
 
         internal bool ThrowWriteExceptions => RequestContext.Server.Settings.ThrowWriteExceptions;
 
+        internal bool IsDisposed => _disposed;
+
         public override bool CanSeek
         {
             get
diff --git a/test/Microsoft.Net.Http.Server.FunctionalTests/ServerTests.cs b/test/Microsoft.Net.Http.Server.FunctionalTests/ServerTests.cs
index 332774d211..21e60cb3aa 100644
--- a/test/Microsoft.Net.Http.Server.FunctionalTests/ServerTests.cs
+++ b/test/Microsoft.Net.Http.Server.FunctionalTests/ServerTests.cs
@@ -104,6 +104,68 @@ namespace Microsoft.Net.Http.Server
             }
         }
 
+        [Fact]
+        public async Task Server_TokenRegisteredAfterClientDisconnects_CallCanceled()
+        {
+            var interval = TimeSpan.FromSeconds(1);
+            var canceled = new ManualResetEvent(false);
+
+            string address;
+            using (var server = Utilities.CreateHttpServer(out address))
+            {
+                using (var client = new HttpClient())
+                {
+                    var responseTask = client.GetAsync(address);
+
+                    var context = await server.AcceptAsync();
+
+                    client.CancelPendingRequests();
+                    await Assert.ThrowsAsync<TaskCanceledException>(() => responseTask);
+
+                    var ct = context.DisconnectToken;
+                    Assert.True(ct.CanBeCanceled, "CanBeCanceled");
+                    ct.Register(() => canceled.Set());
+                    Assert.True(ct.WaitHandle.WaitOne(interval));
+                    Assert.True(ct.IsCancellationRequested, "IsCancellationRequested");
+
+                    Assert.True(canceled.WaitOne(interval), "canceled");
+
+                    context.Dispose();
+                }
+            }
+        }
+
+        [Fact]
+        public async Task Server_TokenRegisteredAfterResponseSent_Success()
+        {
+            var interval = TimeSpan.FromSeconds(1);
+            var canceled = new ManualResetEvent(false);
+
+            string address;
+            using (var server = Utilities.CreateHttpServer(out address))
+            {
+                using (var client = new HttpClient())
+                {
+                    var responseTask = client.GetAsync(address);
+
+                    var context = await server.AcceptAsync();
+                    context.Dispose();
+
+                    var response = await responseTask;
+                    response.EnsureSuccessStatusCode();
+                    Assert.Equal(string.Empty, await response.Content.ReadAsStringAsync());
+
+                    var ct = context.DisconnectToken;
+                    Assert.False(ct.CanBeCanceled, "CanBeCanceled");
+                    ct.Register(() => canceled.Set());
+                    Assert.False(ct.WaitHandle.WaitOne(interval));
+                    Assert.False(ct.IsCancellationRequested, "IsCancellationRequested");
+
+                    Assert.False(canceled.WaitOne(interval), "canceled");
+                }
+            }
+        }
+
         [Fact]
         public async Task Server_Abort_CallCanceled()
         {