diff --git a/src/libraries/Common/src/Interop/Windows/WinHttp/Interop.winhttp_types.cs b/src/libraries/Common/src/Interop/Windows/WinHttp/Interop.winhttp_types.cs
index 27213cc2a0ed39..99bcc38f0a7159 100644
--- a/src/libraries/Common/src/Interop/Windows/WinHttp/Interop.winhttp_types.cs
+++ b/src/libraries/Common/src/Interop/Windows/WinHttp/Interop.winhttp_types.cs
@@ -168,6 +168,7 @@ internal static partial class WinHttp
 
         public const uint WINHTTP_OPTION_TCP_KEEPALIVE = 152;
         public const uint WINHTTP_OPTION_STREAM_ERROR_CODE = 159;
+        public const uint WINHTTP_OPTION_REQUIRE_STREAM_END = 160;
 
         public enum WINHTTP_WEB_SOCKET_BUFFER_TYPE
         {
diff --git a/src/libraries/System.Net.Http.WinHttpHandler/src/System/Net/Http/WinHttpHandler.cs b/src/libraries/System.Net.Http.WinHttpHandler/src/System/Net/Http/WinHttpHandler.cs
index 3b4c247b8b7032..07133b2667c229 100644
--- a/src/libraries/System.Net.Http.WinHttpHandler/src/System/Net/Http/WinHttpHandler.cs
+++ b/src/libraries/System.Net.Http.WinHttpHandler/src/System/Net/Http/WinHttpHandler.cs
@@ -1120,6 +1120,7 @@ private void SetSessionHandleOptions(SafeWinHttpHandle sessionHandle)
             SetSessionHandleTimeoutOptions(sessionHandle);
             SetDisableHttp2StreamQueue(sessionHandle);
             SetTcpKeepalive(sessionHandle);
+            SetRequireStreamEnd(sessionHandle);
         }
 
         private unsafe void SetTcpKeepalive(SafeWinHttpHandle sessionHandle)
@@ -1145,6 +1146,27 @@ private unsafe void SetTcpKeepalive(SafeWinHttpHandle sessionHandle)
             }
         }
 
+        private void SetRequireStreamEnd(SafeWinHttpHandle sessionHandle)
+        {
+            if (WinHttpTrailersHelper.OsSupportsTrailers)
+            {
+                // Setting WINHTTP_OPTION_REQUIRE_STREAM_END to TRUE is needed for WinHttp to read trailing headers
+                // in case the response has Content-Lenght defined.
+                // According to the WinHttp team, the feature-detection logic in WinHttpTrailersHelper.OsSupportsTrailers
+                // should also indicate the support of WINHTTP_OPTION_REQUIRE_STREAM_END.
+                // WINHTTP_OPTION_REQUIRE_STREAM_END doesn't have effect on HTTP 1.1 requests, therefore it's safe to set it on
+                // the session handle so it is inhereted by all request handles.
+                uint optionData = 1;
+                if (!Interop.WinHttp.WinHttpSetOption(sessionHandle, Interop.WinHttp.WINHTTP_OPTION_REQUIRE_STREAM_END, ref optionData))
+                {
+                    if (NetEventSource.Log.IsEnabled())
+                    {
+                        NetEventSource.Info(this, "Failed to enable WINHTTP_OPTION_REQUIRE_STREAM_END error code: " + Marshal.GetLastWin32Error());
+                    }
+                }
+            }
+        }
+
         private void SetSessionHandleConnectionOptions(SafeWinHttpHandle sessionHandle)
         {
             uint optionData = (uint)_maxConnectionsPerServer;
diff --git a/src/libraries/System.Net.Http.WinHttpHandler/tests/FunctionalTests/TrailingHeadersTest.cs b/src/libraries/System.Net.Http.WinHttpHandler/tests/FunctionalTests/TrailingHeadersTest.cs
index cef52465524dcf..5ac753c266ee0a 100644
--- a/src/libraries/System.Net.Http.WinHttpHandler/tests/FunctionalTests/TrailingHeadersTest.cs
+++ b/src/libraries/System.Net.Http.WinHttpHandler/tests/FunctionalTests/TrailingHeadersTest.cs
@@ -67,8 +67,10 @@ public async Task Http2GetAsync_NoTrailingHeaders_EmptyCollection()
             }
         }
 
-        [ConditionalFact(nameof(TestsEnabled))]
-        public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted()
+        [InlineData(false)]
+        [InlineData(true)]
+        [ConditionalTheory(nameof(TestsEnabled))]
+        public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted(bool responseHasContentLength)
         {
             using (Http2LoopbackServer server = Http2LoopbackServer.CreateServer())
             using (HttpClient client = CreateHttpClient())
@@ -80,7 +82,14 @@ public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted()
                 int streamId = await connection.ReadRequestHeaderAsync();
 
                 // Response header.
-                await connection.SendDefaultResponseHeadersAsync(streamId);
+                if (responseHasContentLength)
+                {
+                    await connection.SendResponseHeadersAsync(streamId, endStream: false, headers: new[] { new HttpHeaderData("Content-Length", DataBytes.Length.ToString()) });
+                }
+                else
+                {
+                    await connection.SendDefaultResponseHeadersAsync(streamId);
+                }
 
                 // Response data, missing Trailers.
                 await connection.WriteFrameAsync(MakeDataFrame(streamId, DataBytes));
@@ -98,8 +107,10 @@ public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted()
             }
         }
 
-        [ConditionalFact(nameof(TestsEnabled))]
-        public async Task Http2GetAsyncResponseHeadersReadOption_TrailingHeaders_Available()
+        [InlineData(false)]
+        [InlineData(true)]
+        [ConditionalTheory(nameof(TestsEnabled))]
+        public async Task Http2GetAsyncResponseHeadersReadOption_TrailingHeaders_Available(bool responseHasContentLength)
         {
             using (Http2LoopbackServer server = Http2LoopbackServer.CreateServer())
             using (HttpClient client = CreateHttpClient())
@@ -111,7 +122,14 @@ public async Task Http2GetAsyncResponseHeadersReadOption_TrailingHeaders_Availab
                 int streamId = await connection.ReadRequestHeaderAsync();
 
                 // Response header.
-                await connection.SendDefaultResponseHeadersAsync(streamId);
+                if (responseHasContentLength)
+                {
+                    await connection.SendResponseHeadersAsync(streamId, endStream: false, headers: new[] { new HttpHeaderData("Content-Length", DataBytes.Length.ToString()) });
+                }
+                else
+                {
+                    await connection.SendDefaultResponseHeadersAsync(streamId);
+                }
 
                 // Response data, missing Trailers.
                 await connection.WriteFrameAsync(MakeDataFrame(streamId, DataBytes));
diff --git a/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs b/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
index 14f444b1935a60..bfd1e83bfad502 100644
--- a/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
+++ b/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
@@ -837,8 +837,10 @@ public async Task Http2GetAsync_NoTrailingHeaders_EmptyCollection()
             }
         }
 
-        [ConditionalFact(typeof(PlatformDetection), nameof(PlatformDetection.SupportsAlpn))]
-        public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted()
+        [InlineData(false)]
+        [InlineData(true)]
+        [ConditionalTheory(typeof(PlatformDetection), nameof(PlatformDetection.SupportsAlpn))]
+        public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted(bool responseHasContentLength)
         {
             using (Http2LoopbackServer server = Http2LoopbackServer.CreateServer())
             using (HttpClient client = CreateHttpClient())
@@ -850,7 +852,14 @@ public async Task Http2GetAsync_MissingTrailer_TrailingHeadersAccepted()
                 int streamId = await connection.ReadRequestHeaderAsync();
 
                 // Response header.
-                await connection.SendDefaultResponseHeadersAsync(streamId);
+                if (responseHasContentLength)
+                {
+                    await connection.SendResponseHeadersAsync(streamId, endStream: false, headers: new[] { new HttpHeaderData("Content-Length", DataBytes.Length.ToString()) });
+                }
+                else
+                {
+                    await connection.SendDefaultResponseHeadersAsync(streamId);
+                }
 
                 // Response data, missing Trailers.
                 await connection.WriteFrameAsync(MakeDataFrame(streamId, DataBytes));
@@ -888,8 +897,10 @@ public async Task Http2GetAsync_TrailerHeaders_TrailingPseudoHeadersThrow()
             }
         }
 
-        [ConditionalFact(typeof(PlatformDetection), nameof(PlatformDetection.SupportsAlpn))]
-        public async Task Http2GetAsyncResponseHeadersReadOption_TrailingHeaders_Available()
+        [InlineData(false)]
+        [InlineData(true)]
+        [ConditionalTheory(typeof(PlatformDetection), nameof(PlatformDetection.SupportsAlpn))]
+        public async Task Http2GetAsyncResponseHeadersReadOption_TrailingHeaders_Available(bool responseHasContentLength)
         {
             using (Http2LoopbackServer server = Http2LoopbackServer.CreateServer())
             using (HttpClient client = CreateHttpClient())
@@ -901,7 +912,14 @@ public async Task Http2GetAsyncResponseHeadersReadOption_TrailingHeaders_Availab
                 int streamId = await connection.ReadRequestHeaderAsync();
 
                 // Response header.
-                await connection.SendDefaultResponseHeadersAsync(streamId);
+                if (responseHasContentLength)
+                {
+                    await connection.SendResponseHeadersAsync(streamId, endStream: false, headers: new[] { new HttpHeaderData("Content-Length", DataBytes.Length.ToString()) });
+                }
+                else
+                {
+                    await connection.SendDefaultResponseHeadersAsync(streamId);
+                }
 
                 // Response data, missing Trailers.
                 await connection.WriteFrameAsync(MakeDataFrame(streamId, DataBytes));