diff --git a/src/libraries/System.Net.Quic/src/System/Net/Quic/Internal/ThrowHelper.cs b/src/libraries/System.Net.Quic/src/System/Net/Quic/Internal/ThrowHelper.cs
index ec677f9f4e58d..e99f5fda640e1 100644
--- a/src/libraries/System.Net.Quic/src/System/Net/Quic/Internal/ThrowHelper.cs
+++ b/src/libraries/System.Net.Quic/src/System/Net/Quic/Internal/ThrowHelper.cs
@@ -27,13 +27,27 @@ internal static QuicException GetOperationAbortedException(string? message = nul
         return new QuicException(QuicError.OperationAborted, null, message ?? SR.net_quic_operationaborted);
     }
 
-    internal static bool TryGetStreamExceptionForMsQuicStatus(int status, [NotNullWhen(true)] out Exception? exception)
+    internal static bool TryGetStreamExceptionForMsQuicStatus(int status, [NotNullWhen(true)] out Exception? exception, bool streamWasSuccessfullyStarted = true, string? message = null)
     {
         if (status == QUIC_STATUS_ABORTED)
         {
-            // If status == QUIC_STATUS_ABORTED, we will receive an event later, which will complete the task source.
-            exception = null;
-            return false;
+            // Connection has been closed by the peer (either at transport or application level),
+            if (streamWasSuccessfullyStarted)
+            {
+                // we will receive an event later, which will complete the stream with concrete
+                // information why the connection was aborted.
+                exception = null;
+                return false;
+            }
+            else
+            {
+                // we won't be receiving any event callback for shutdown on this stream, so we don't
+                // necessarily know which error to report. So we throw an exception which we can distinguish
+                // at the caller (ConnectionAborted normally has App error code) and throw the correct
+                // exception from there.
+                exception = new QuicException(QuicError.ConnectionAborted, null, "");
+                return true;
+            }
         }
         else if (status == QUIC_STATUS_INVALID_STATE)
         {
@@ -43,13 +57,16 @@ internal static bool TryGetStreamExceptionForMsQuicStatus(int status, [NotNullWh
         }
         else if (StatusFailed(status))
         {
-            exception = GetExceptionForMsQuicStatus(status);
+            exception = GetExceptionForMsQuicStatus(status, message: message);
             return true;
         }
         exception = null;
         return false;
     }
 
+    // see TryGetStreamExceptionForMsQuicStatus for explanation
+    internal static bool IsConnectionAbortedWhenStartingStreamException(Exception ex) => ex is QuicException qe && qe.QuicError == QuicError.ConnectionAborted && qe.ApplicationErrorCode is null;
+
     internal static Exception GetExceptionForMsQuicStatus(int status, long? errorCode = default, string? message = null)
     {
         Exception ex = GetExceptionInternal(status, errorCode, message);
diff --git a/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicConnection.cs b/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicConnection.cs
index a2ade033afe59..13351faaa20c0 100644
--- a/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicConnection.cs
+++ b/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicConnection.cs
@@ -98,6 +98,11 @@ static async ValueTask<QuicConnection> StartConnectAsync(QuicClientConnectionOpt
     /// </summary>
     private int _disposed;
 
+    /// <summary>
+    /// Completed when connection shutdown is initiated.
+    /// </summary>
+    private TaskCompletionSource _connectionCloseTcs = new TaskCompletionSource(TaskCreationOptions.RunContinuationsAsynchronously);
+
     private readonly ValueTaskSource _connectedTcs = new ValueTaskSource();
     private readonly ValueTaskSource _shutdownTcs = new ValueTaskSource();
 
@@ -376,16 +381,22 @@ public async ValueTask<QuicStream> OpenOutboundStreamAsync(QuicStreamType type,
             stream = new QuicStream(_handle, type, _defaultStreamErrorCode);
             await stream.StartAsync(cancellationToken).ConfigureAwait(false);
         }
-        catch
+        catch (Exception ex)
         {
             if (stream is not null)
             {
                 await stream.DisposeAsync().ConfigureAwait(false);
             }
+
+            // In case of an incoming race when the connection is closed by the peer just before we open the stream,
+            // we receive QUIC_STATUS_ABORTED from MsQuic, but we don't know how the connection was closed. We throw
+            // special exception and handle it here where we can determine the shutdown reason.
+            bool connectionAbortedByPeer = ThrowHelper.IsConnectionAbortedWhenStartingStreamException(ex);
+
             // Propagate connection error if present.
-            if (_acceptQueue.Reader.Completion.IsFaulted)
+            if (_connectionCloseTcs.Task.IsFaulted || connectionAbortedByPeer)
             {
-                await _acceptQueue.Reader.Completion.ConfigureAwait(false);
+                await _connectionCloseTcs.Task.ConfigureAwait(false);
             }
             throw;
         }
@@ -475,17 +486,21 @@ private unsafe int HandleEventShutdownInitiatedByTransport(ref SHUTDOWN_INITIATE
     {
         Exception exception = ExceptionDispatchInfo.SetCurrentStackTrace(ThrowHelper.GetExceptionForMsQuicStatus(data.Status, (long)data.ErrorCode));
         _connectedTcs.TrySetException(exception);
+        _connectionCloseTcs.TrySetException(exception);
         _acceptQueue.Writer.TryComplete(exception);
         return QUIC_STATUS_SUCCESS;
     }
     private unsafe int HandleEventShutdownInitiatedByPeer(ref SHUTDOWN_INITIATED_BY_PEER_DATA data)
     {
-        _acceptQueue.Writer.TryComplete(ExceptionDispatchInfo.SetCurrentStackTrace(ThrowHelper.GetConnectionAbortedException((long)data.ErrorCode)));
+        Exception exception = ExceptionDispatchInfo.SetCurrentStackTrace(ThrowHelper.GetConnectionAbortedException((long)data.ErrorCode));
+        _connectionCloseTcs.TrySetException(exception);
+        _acceptQueue.Writer.TryComplete(exception);
         return QUIC_STATUS_SUCCESS;
     }
     private unsafe int HandleEventShutdownComplete()
     {
         Exception exception = ExceptionDispatchInfo.SetCurrentStackTrace(ThrowHelper.GetOperationAbortedException());
+        _connectionCloseTcs.TrySetException(exception);
         _acceptQueue.Writer.TryComplete(exception);
         _connectedTcs.TrySetException(exception);
         _shutdownTcs.TrySetResult();
diff --git a/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicStream.cs b/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicStream.cs
index 6165f2085cb5f..82ee656dc6bdc 100644
--- a/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicStream.cs
+++ b/src/libraries/System.Net.Quic/src/System/Net/Quic/QuicStream.cs
@@ -161,13 +161,18 @@ internal unsafe QuicStream(MsQuicContextSafeHandle connectionHandle, QuicStreamT
         try
         {
             QUIC_HANDLE* handle;
-            ThrowHelper.ThrowIfMsQuicError(MsQuicApi.Api.StreamOpen(
+            int status = MsQuicApi.Api.StreamOpen(
                 connectionHandle,
                 type == QuicStreamType.Unidirectional ? QUIC_STREAM_OPEN_FLAGS.UNIDIRECTIONAL : QUIC_STREAM_OPEN_FLAGS.NONE,
                 &NativeCallback,
                 (void*)GCHandle.ToIntPtr(context),
-                &handle),
-                "StreamOpen failed");
+                &handle);
+
+            if (ThrowHelper.TryGetStreamExceptionForMsQuicStatus(status, out Exception? ex, streamWasSuccessfullyStarted: false, message: "StreamOpen failed"))
+            {
+                throw ex;
+            }
+
             _handle = new MsQuicContextSafeHandle(handle, context, SafeHandleType.Stream, connectionHandle);
         }
         catch
@@ -241,7 +246,8 @@ internal ValueTask StartAsync(CancellationToken cancellationToken = default)
                 int status = MsQuicApi.Api.StreamStart(
                     _handle,
                     QUIC_STREAM_START_FLAGS.SHUTDOWN_ON_FAIL | QUIC_STREAM_START_FLAGS.INDICATE_PEER_ACCEPT);
-                if (ThrowHelper.TryGetStreamExceptionForMsQuicStatus(status, out Exception? exception))
+
+                if (ThrowHelper.TryGetStreamExceptionForMsQuicStatus(status, out Exception? exception, streamWasSuccessfullyStarted: false))
                 {
                     _startedTcs.TrySetException(exception);
                 }