diff --git a/src/Servers/Kestrel/Transport.Sockets/src/SocketConnectionListener.cs b/src/Servers/Kestrel/Transport.Sockets/src/SocketConnectionListener.cs
index 4c49a90233..a98ec04363 100644
--- a/src/Servers/Kestrel/Transport.Sockets/src/SocketConnectionListener.cs
+++ b/src/Servers/Kestrel/Transport.Sockets/src/SocketConnectionListener.cs
@@ -3,7 +3,6 @@
 
 using System;
 using System.Buffers;
-using System.Diagnostics;
 using System.IO.Pipelines;
 using System.Net;
 using System.Net.Sockets;
@@ -23,6 +22,7 @@ namespace Microsoft.AspNetCore.Server.Kestrel.Transport.Sockets
         private Socket _listenSocket;
         private int _schedulerIndex;
         private readonly SocketTransportOptions _options;
+        private SafeSocketHandle _socketHandle;
 
         public EndPoint EndPoint { get; private set; }
 
@@ -62,33 +62,44 @@ namespace Microsoft.AspNetCore.Server.Kestrel.Transport.Sockets
                 throw new InvalidOperationException(SocketsStrings.TransportAlreadyBound);
             }
 
-            // Check if EndPoint is a FileHandleEndpoint before attempting to access EndPoint.AddressFamily
-            // since that will throw an NotImplementedException.
-            if (EndPoint is FileHandleEndPoint)
-            {
-                throw new NotSupportedException(SocketsStrings.FileHandleEndPointNotSupported);
-            }
-
             Socket listenSocket;
 
-            // Unix domain sockets are unspecified
-            var protocolType = EndPoint is UnixDomainSocketEndPoint ? ProtocolType.Unspecified : ProtocolType.Tcp;
-
-            listenSocket = new Socket(EndPoint.AddressFamily, SocketType.Stream, protocolType);
-
-            // Kestrel expects IPv6Any to bind to both IPv6 and IPv4
-            if (EndPoint is IPEndPoint ip && ip.Address == IPAddress.IPv6Any)
+            switch (EndPoint)
             {
-                listenSocket.DualMode = true;
+                case FileHandleEndPoint fileHandle:
+                    _socketHandle = new SafeSocketHandle((IntPtr)fileHandle.FileHandle, ownsHandle: true);
+                    listenSocket = new Socket(_socketHandle);
+                    break;
+                case UnixDomainSocketEndPoint unix:
+                    listenSocket = new Socket(unix.AddressFamily, SocketType.Stream, ProtocolType.Unspecified);
+                    BindSocket();
+                    break;
+                case IPEndPoint ip:
+                    listenSocket = new Socket(ip.AddressFamily, SocketType.Stream, ProtocolType.Tcp);
+
+                    // Kestrel expects IPv6Any to bind to both IPv6 and IPv4
+                    if (ip.Address == IPAddress.IPv6Any)
+                    {
+                        listenSocket.DualMode = true;
+                    }
+                    BindSocket();
+                    break;
+                default:
+                    listenSocket = new Socket(EndPoint.AddressFamily, SocketType.Stream, ProtocolType.Tcp);
+                    BindSocket();
+                    break;
             }
 
-            try
+            void BindSocket()
             {
-                listenSocket.Bind(EndPoint);
-            }
-            catch (SocketException e) when (e.SocketErrorCode == SocketError.AddressAlreadyInUse)
-            {
-                throw new AddressInUseException(e.Message, e);
+                try
+                {
+                    listenSocket.Bind(EndPoint);
+                }
+                catch (SocketException e) when (e.SocketErrorCode == SocketError.AddressAlreadyInUse)
+                {
+                    throw new AddressInUseException(e.Message, e);
+                }
             }
 
             EndPoint = listenSocket.LocalEndPoint;
@@ -142,12 +153,17 @@ namespace Microsoft.AspNetCore.Server.Kestrel.Transport.Sockets
         public ValueTask UnbindAsync(CancellationToken cancellationToken = default)
         {
             _listenSocket?.Dispose();
+
+            _socketHandle?.Dispose();
             return default;
         }
 
         public ValueTask DisposeAsync()
         {
             _listenSocket?.Dispose();
+
+            _socketHandle?.Dispose();
+
             // Dispose the memory pool
             _memoryPool.Dispose();
             return default;
diff --git a/src/Servers/Kestrel/test/Libuv.FunctionalTests/ListenHandleTests.cs b/src/Servers/Kestrel/test/FunctionalTests/ListenHandleTests.cs
similarity index 97%
rename from src/Servers/Kestrel/test/Libuv.FunctionalTests/ListenHandleTests.cs
rename to src/Servers/Kestrel/test/FunctionalTests/ListenHandleTests.cs
index 672e55dc7d..a9cac6f788 100644
--- a/src/Servers/Kestrel/test/Libuv.FunctionalTests/ListenHandleTests.cs
+++ b/src/Servers/Kestrel/test/FunctionalTests/ListenHandleTests.cs
@@ -1,12 +1,14 @@
 // 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;
 using System.Net;
 using System.Net.Sockets;
 using System.Threading.Tasks;
+using Microsoft.AspNetCore.Connections;
 using Microsoft.AspNetCore.Server.Kestrel.Core;
 using Microsoft.AspNetCore.Testing;
-using Microsoft.Extensions.Logging.Testing;
+using Xunit;
 
 namespace Microsoft.AspNetCore.Server.Kestrel.FunctionalTests
 {
diff --git a/src/Servers/Kestrel/test/Sockets.BindTests/SocketTransportFactoryTests.cs b/src/Servers/Kestrel/test/Sockets.BindTests/SocketTransportFactoryTests.cs
index b67e2dfcaa..77acddd957 100644
--- a/src/Servers/Kestrel/test/Sockets.BindTests/SocketTransportFactoryTests.cs
+++ b/src/Servers/Kestrel/test/Sockets.BindTests/SocketTransportFactoryTests.cs
@@ -14,13 +14,6 @@ namespace Sockets.BindTests
 {
     public class SocketTransportFactoryTests
     {
-        [Fact]
-        public async Task ThrowsNotSupportedExceptionWhenBindingToFileHandleEndPoint()
-        {
-            var socketTransportFactory = new SocketTransportFactory(Options.Create(new SocketTransportOptions()), Mock.Of<ILoggerFactory>());
-            await Assert.ThrowsAsync<NotSupportedException>(async () => await socketTransportFactory.BindAsync(new FileHandleEndPoint(0, FileHandleType.Auto)));
-        }
-
         [Fact]
         public async Task ThrowsNotImplementedExceptionWhenBindingToUriEndPoint()
         {