diff --git a/src/Servers/HttpSys/src/DelegationRule.cs b/src/Servers/HttpSys/src/DelegationRule.cs
index e33997338c..70b85c7c22 100644
--- a/src/Servers/HttpSys/src/DelegationRule.cs
+++ b/src/Servers/HttpSys/src/DelegationRule.cs
@@ -13,6 +13,8 @@ namespace Microsoft.AspNetCore.Server.HttpSys
     public class DelegationRule : IDisposable
     {
         private readonly ILogger _logger;
+        private readonly UrlGroup _sourceQueueUrlGroup;
+        private bool _disposed;
         /// <summary>
         /// The name of the Http.Sys request queue
         /// </summary>
@@ -23,8 +25,9 @@ namespace Microsoft.AspNetCore.Server.HttpSys
         public string UrlPrefix { get; }
         internal RequestQueue Queue { get; }
 
-        internal DelegationRule(string queueName, string urlPrefix, ILogger logger)
+        internal DelegationRule(UrlGroup sourceQueueUrlGroup, string queueName, string urlPrefix, ILogger logger)
         {
+            _sourceQueueUrlGroup = sourceQueueUrlGroup;
             _logger = logger;
             QueueName = queueName;
             UrlPrefix = urlPrefix;
@@ -34,8 +37,20 @@ namespace Microsoft.AspNetCore.Server.HttpSys
         /// <inheritdoc />
         public void Dispose()
         {
-            Queue.UrlGroup?.Dispose();
-            Queue?.Dispose();
+            if (_disposed)
+            {
+                return;
+            }
+
+            _disposed = true;
+
+            try
+            {
+                _sourceQueueUrlGroup.UnSetDelegationProperty(Queue, throwOnError: false);
+            }
+            catch (ObjectDisposedException) { /* Server may have been shutdown */ }
+            Queue.UrlGroup.Dispose();
+            Queue.Dispose();
         }
     }
 }
diff --git a/src/Servers/HttpSys/src/NativeInterop/UrlGroup.cs b/src/Servers/HttpSys/src/NativeInterop/UrlGroup.cs
index ea6c657813..d93d236477 100644
--- a/src/Servers/HttpSys/src/NativeInterop/UrlGroup.cs
+++ b/src/Servers/HttpSys/src/NativeInterop/UrlGroup.cs
@@ -83,6 +83,15 @@ namespace Microsoft.AspNetCore.Server.HttpSys
             SetProperty(HttpApiTypes.HTTP_SERVER_PROPERTY.HttpServerDelegationProperty, new IntPtr(&propertyInfo), (uint)RequestPropertyInfoSize);
         }
 
+        internal unsafe void UnSetDelegationProperty(RequestQueue destination, bool throwOnError = true)
+        {
+            var propertyInfo = new HttpApiTypes.HTTP_BINDING_INFO();
+            propertyInfo.Flags = HttpApiTypes.HTTP_FLAGS.NONE;
+            propertyInfo.RequestQueueHandle = destination.Handle.DangerousGetHandle();
+
+            SetProperty(HttpApiTypes.HTTP_SERVER_PROPERTY.HttpServerDelegationProperty, new IntPtr(&propertyInfo), (uint)RequestPropertyInfoSize, throwOnError);
+        }
+
         internal void SetProperty(HttpApiTypes.HTTP_SERVER_PROPERTY property, IntPtr info, uint infosize, bool throwOnError = true)
         {
             Debug.Assert(info != IntPtr.Zero, "SetUrlGroupProperty called with invalid pointer");
diff --git a/src/Servers/HttpSys/src/ServerDelegationPropertyFeature.cs b/src/Servers/HttpSys/src/ServerDelegationPropertyFeature.cs
index d9066a3dd5..07041f08d2 100644
--- a/src/Servers/HttpSys/src/ServerDelegationPropertyFeature.cs
+++ b/src/Servers/HttpSys/src/ServerDelegationPropertyFeature.cs
@@ -21,7 +21,7 @@ namespace Microsoft.AspNetCore.Server.HttpSys
 
         public DelegationRule CreateDelegationRule(string queueName, string uri)
         {
-            var rule = new DelegationRule(queueName, uri, _logger);
+            var rule = new DelegationRule(_queue.UrlGroup, queueName, uri, _logger);
             _queue.UrlGroup.SetDelegationProperty(rule.Queue);
             return rule;
         }
diff --git a/src/Servers/HttpSys/test/FunctionalTests/DelegateTests.cs b/src/Servers/HttpSys/test/FunctionalTests/DelegateTests.cs
index f94f0bf0be..de896ed679 100644
--- a/src/Servers/HttpSys/test/FunctionalTests/DelegateTests.cs
+++ b/src/Servers/HttpSys/test/FunctionalTests/DelegateTests.cs
@@ -161,6 +161,38 @@ namespace Microsoft.AspNetCore.Server.HttpSys.FunctionalTests
             _ = await SendRequestAsync(delegatorAddress);
         }
 
+        [ConditionalFact]
+        [DelegateSupportedCondition(true)]
+        public async Task UpdateDelegationRuleTest()
+        {
+            var queueName = Guid.NewGuid().ToString();
+            using var receiver = Utilities.CreateHttpServer(out var receiverAddress, async httpContext =>
+            {
+                await httpContext.Response.WriteAsync(_expectedResponseString);
+            },
+           options =>
+           {
+               options.RequestQueueName = queueName;
+           });
+
+            DelegationRule destination = default;
+
+            using var delegator = Utilities.CreateHttpServer(out var delegatorAddress, httpContext =>
+            {
+                var delegateFeature = httpContext.Features.Get<IHttpSysRequestDelegationFeature>();
+                delegateFeature.DelegateRequest(destination);
+                return Task.CompletedTask;
+            });
+
+            var delegationProperty = delegator.Features.Get<IServerDelegationFeature>();
+            destination = delegationProperty.CreateDelegationRule(queueName, receiverAddress);
+            destination?.Dispose();
+            destination = delegationProperty.CreateDelegationRule(queueName, receiverAddress);
+            var responseString = await SendRequestAsync(delegatorAddress);
+            Assert.Equal(_expectedResponseString, responseString);
+            destination?.Dispose();
+        }
+
         private async Task<string> SendRequestAsync(string uri)
         {
             using var client = new HttpClient();