diff --git a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http3RequestStream.cs b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http3RequestStream.cs
index fcfbfa8e6df786..c49cf1d195d438 100644
--- a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http3RequestStream.cs
+++ b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http3RequestStream.cs
@@ -566,14 +566,9 @@ private async ValueTask DrainContentLength0Frames(CancellationToken cancellation
                 switch (frameType)
                 {
                     case Http3FrameType.Headers:
-                        // Pick up any trailing headers.
-                        _trailingHeaders = new List<(HeaderDescriptor name, string value)>();
-                        await ReadHeadersAsync(payloadLength, cancellationToken).ConfigureAwait(false);
-
-                        // Stop looping after a trailing header.
-                        // There may be extra frames after this one, but they would all be unknown extension
-                        // frames that can be safely ignored. Just stop reading here.
-                        // Note: this does leave us open to a bad server sending us an out of order DATA frame.
+                        // Pick up any trailing headers and stop processing.
+                        await ProcessTrailersAsync(payloadLength, cancellationToken).ConfigureAwait(false);
+
                         goto case null;
                     case null:
                         // Done receiving: copy over trailing headers.
@@ -601,6 +596,25 @@ private async ValueTask DrainContentLength0Frames(CancellationToken cancellation
             }
         }
 
+        private async ValueTask ProcessTrailersAsync(long payloadLength, CancellationToken cancellationToken)
+        {
+            _trailingHeaders = new List<(HeaderDescriptor name, string value)>();
+            await ReadHeadersAsync(payloadLength, cancellationToken).ConfigureAwait(false);
+
+            // In typical cases, there should be no more frames. Make sure to read the EOS.
+            _recvBuffer.EnsureAvailableSpace(1);
+            int bytesRead = await _stream.ReadAsync(_recvBuffer.AvailableMemory, cancellationToken).ConfigureAwait(false);
+            if (bytesRead > 0)
+            {
+                // The server may send us frames of unknown types after the trailer. Ideally we should drain the response by eating and ignoring them
+                // but this is a rare case so we just stop reading and let Dispose() send an ABORT_RECEIVE.
+                // Note: if a server sends additional HEADERS or DATA frames at this point, it
+                // would be a connection error -- not draining the stream also means we won't catch this.
+                _recvBuffer.Commit(bytesRead);
+                _recvBuffer.Discard(bytesRead);
+            }
+        }
+
         private void CopyTrailersToResponseMessage(HttpResponseMessage responseMessage)
         {
             if (_trailingHeaders?.Count > 0)
@@ -1367,15 +1381,9 @@ private async ValueTask<bool> ReadNextDataFrameAsync(HttpResponseMessage respons
                         _responseDataPayloadRemaining = payloadLength;
                         return true;
                     case Http3FrameType.Headers:
-                        // Read any trailing headers.
-                        _trailingHeaders = new List<(HeaderDescriptor name, string value)>();
-                        await ReadHeadersAsync(payloadLength, cancellationToken).ConfigureAwait(false);
-
-                        // There may be more frames after this one, but they would all be unknown extension
-                        // frames that we are allowed to skip. Just close the stream early.
+                        // Pick up any trailing headers and stop processing.
+                        await ProcessTrailersAsync(payloadLength, cancellationToken).ConfigureAwait(false);
 
-                        // Note: if a server sends additional HEADERS or DATA frames at this point, it
-                        // would be a connection error -- not draining the stream means we won't catch this.
                         goto case null;
                     case null:
                         // End of stream.
diff --git a/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs b/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
index 478c9ce0c88838..2577094cb52b4e 100644
--- a/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
+++ b/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
@@ -7,11 +7,9 @@
 using System.IO.Pipes;
 using System.Linq;
 using System.Net.Http.Headers;
-using System.Net.Quic;
 using System.Net.Security;
 using System.Net.Sockets;
 using System.Net.Test.Common;
-using System.Numerics;
 using System.Reflection;
 using System.Runtime.CompilerServices;
 using System.Security.Authentication;
@@ -1285,6 +1283,69 @@ protected override async Task AcceptConnectionAndSendResponseAsync(
             await stream.SendResponseHeadersAsync(statusCode: null, headers: trailers);
             stream.Stream.CompleteWrites();
         }
+
+        [Theory]
+        [InlineData(false, HttpCompletionOption.ResponseContentRead)]
+        [InlineData(false, HttpCompletionOption.ResponseHeadersRead)]
+        [InlineData(true, HttpCompletionOption.ResponseContentRead)]
+        [InlineData(true, HttpCompletionOption.ResponseHeadersRead)]
+        public async Task GetAsync_TrailersWithoutServerStreamClosure_Success(bool emptyResponse, HttpCompletionOption httpCompletionOption)
+        {
+            SemaphoreSlim serverCompleted = new SemaphoreSlim(0);
+
+            await LoopbackServerFactory.CreateClientAndServerAsync(async uri =>
+            {
+                HttpClientHandler handler = CreateHttpClientHandler();
+
+                // Avoid drain timeout if CI is slow.
+                GetUnderlyingSocketsHttpHandler(handler).ResponseDrainTimeout = TimeSpan.FromSeconds(10);
+                using HttpClient client = CreateHttpClient(handler);
+
+                using (HttpResponseMessage response = await client.GetAsync(uri, httpCompletionOption))
+                {
+                    if (httpCompletionOption == HttpCompletionOption.ResponseHeadersRead)
+                    {
+                        using Stream stream = await response.Content.ReadAsStreamAsync();
+                        byte[] buffer = new byte[512];
+                        // Consume the stream
+                        while ((await stream.ReadAsync(buffer)) > 0) ;
+                    }
+
+                    Assert.Equal(TrailingHeaders.Count, response.TrailingHeaders.Count());
+                }
+
+                await serverCompleted.WaitAsync();
+            },
+            async server =>
+            {
+                try
+                {
+                    await using Http3LoopbackConnection connection = (Http3LoopbackConnection)await server.EstablishGenericConnectionAsync();
+                    await using Http3LoopbackStream stream = await connection.AcceptRequestStreamAsync();
+                    _ = await stream.ReadRequestDataAsync();
+
+                    HttpHeaderData[] headers = emptyResponse ? [new HttpHeaderData("Content-Length", "0")] : null;
+
+                    await stream.SendResponseHeadersAsync(statusCode: HttpStatusCode.OK, headers);
+                    if (!emptyResponse)
+                    {
+                        await stream.SendResponseBodyAsync(new byte[16384], isFinal: false);
+                    }
+
+                    await stream.SendResponseHeadersAsync(statusCode: null, headers: TrailingHeaders);
+
+                    // Small delay to make sure we do test if the client is waiting for EOS.
+                    await Task.Delay(15);
+
+                    await stream.DisposeAsync();
+                    await stream.Stream.WritesClosed;
+                }
+                finally
+                {
+                    serverCompleted.Release();
+                }
+            }).WaitAsync(TimeSpan.FromSeconds(30));
+        }
     }
 
     public sealed class SocketsHttpHandler_HttpClientHandlerTest : HttpClientHandlerTest