diff --git a/src/Servers/Kestrel/Core/src/Internal/Http2/Http2Connection.cs b/src/Servers/Kestrel/Core/src/Internal/Http2/Http2Connection.cs
index 05321d3e73e1..64880e0dfb0f 100644
--- a/src/Servers/Kestrel/Core/src/Internal/Http2/Http2Connection.cs
+++ b/src/Servers/Kestrel/Core/src/Internal/Http2/Http2Connection.cs
@@ -1156,8 +1156,12 @@ private Task ProcessWindowUpdateFrameAsync()
         {
             if (stream.RstStreamReceived)
             {
-                // Hard abort, do not allow any more frames on this stream.
-                throw CreateReceivedFrameStreamAbortedException(stream);
+                // WINDOW_UPDATE received after we have already processed an inbound RST_STREAM for this stream.
+                // RFC 7540 (Sections 5.1, 6.9) / RFC 9113 do not explicitly define semantics for WINDOW_UPDATE on a
+                // stream in the "closed" state due to a reset by client. We surface it as a stream error (STREAM_CLOSED)
+                // rather than aborting the entire connection to keep behavior deterministic and consistent with other servers.
+                // https://github.com/dotnet/aspnetcore/issues/63726
+                throw new Http2StreamErrorException(_incomingFrame.StreamId, CoreStrings.Http2StreamAborted, Http2ErrorCode.STREAM_CLOSED);
             }
 
             if (!stream.TryUpdateOutputWindow(_incomingFrame.WindowUpdateSizeIncrement))
diff --git a/src/Servers/Kestrel/test/InMemory.FunctionalTests/Http2/Http2ConnectionTests.cs b/src/Servers/Kestrel/test/InMemory.FunctionalTests/Http2/Http2ConnectionTests.cs
index d858d0dcfd28..e289b6833dc6 100644
--- a/src/Servers/Kestrel/test/InMemory.FunctionalTests/Http2/Http2ConnectionTests.cs
+++ b/src/Servers/Kestrel/test/InMemory.FunctionalTests/Http2/Http2ConnectionTests.cs
@@ -3584,7 +3584,6 @@ public async Task RST_STREAM_IncompleteRequest_AdditionalResetFrame_IgnoreAdditi
         AssertConnectionNoError();
     }
 
-    [QuarantinedTest("https://github.com/dotnet/aspnetcore/issues/53744")]
     [Fact]
     public async Task RST_STREAM_IncompleteRequest_AdditionalWindowUpdateFrame_ConnectionAborted()
     {
@@ -3602,10 +3601,13 @@ public async Task RST_STREAM_IncompleteRequest_AdditionalWindowUpdateFrame_Conne
         await SendDataAsync(1, new byte[1], endStream: false);
         await SendRstStreamAsync(1);
         await SendWindowUpdateAsync(1, 1024);
-        tcs.TrySetResult();
 
-        await WaitForConnectionErrorAsync<Http2ConnectionErrorException>(ignoreNonGoAwayFrames: false, expectedLastStreamId: 1,
-            Http2ErrorCode.STREAM_CLOSED, CoreStrings.FormatHttp2ErrorStreamAborted(Http2FrameType.WINDOW_UPDATE, 1));
+        await WaitForStreamErrorAsync(expectedStreamId: 1, Http2ErrorCode.STREAM_CLOSED, CoreStrings.Http2StreamAborted);
+
+        tcs.TrySetResult(); // Don't let the response start until after the abort
+
+        await StopConnectionAsync(expectedLastStreamId: 1, ignoreNonGoAwayFrames: false);
+        AssertConnectionNoError();
     }
 
     [Fact]