diff --git a/src/libraries/System.Net.Http/src/Resources/Strings.resx b/src/libraries/System.Net.Http/src/Resources/Strings.resx
index a6972e36a6be5b..7464b6aa14086a 100644
--- a/src/libraries/System.Net.Http/src/Resources/Strings.resx
+++ b/src/libraries/System.Net.Http/src/Resources/Strings.resx
@@ -309,6 +309,9 @@
   <data name="net_http_invalid_response" xml:space="preserve">
     <value>The server returned an invalid or unrecognized response.</value>
   </data>
+  <data name="net_http_request_content_length_mismatch" xml:space="preserve">
+    <value>Sent {0} request content bytes, but Content-Length promised {1}.</value>
+  </data>
   <data name="net_http_invalid_response_premature_eof" xml:space="preserve">
     <value>The response ended prematurely.</value>
   </data>
diff --git a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/ContentLengthWriteStream.cs b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/ContentLengthWriteStream.cs
index 5b7b6551661972..33add1358ab51a 100644
--- a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/ContentLengthWriteStream.cs
+++ b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/ContentLengthWriteStream.cs
@@ -11,14 +11,23 @@ internal sealed partial class HttpConnection : IDisposable
     {
         private sealed class ContentLengthWriteStream : HttpContentWriteStream
         {
-            public ContentLengthWriteStream(HttpConnection connection) : base(connection)
+            private readonly long _contentLength;
+
+            public ContentLengthWriteStream(HttpConnection connection, long contentLength)
+                : base(connection)
             {
+                _contentLength = contentLength;
             }
 
             public override void Write(ReadOnlySpan<byte> buffer)
             {
                 BytesWritten += buffer.Length;
 
+                if (BytesWritten > _contentLength)
+                {
+                    throw new HttpRequestException(SR.net_http_content_write_larger_than_content_length);
+                }
+
                 // Have the connection write the data, skipping the buffer. Importantly, this will
                 // force a flush of anything already in the buffer, i.e. any remaining request headers
                 // that are still buffered.
@@ -31,6 +40,11 @@ public override ValueTask WriteAsync(ReadOnlyMemory<byte> buffer, CancellationTo
             {
                 BytesWritten += buffer.Length;
 
+                if (BytesWritten > _contentLength)
+                {
+                    return ValueTask.FromException(new HttpRequestException(SR.net_http_content_write_larger_than_content_length));
+                }
+
                 // Have the connection write the data, skipping the buffer. Importantly, this will
                 // force a flush of anything already in the buffer, i.e. any remaining request headers
                 // that are still buffered.
@@ -41,6 +55,11 @@ public override ValueTask WriteAsync(ReadOnlyMemory<byte> buffer, CancellationTo
 
             public override Task FinishAsync(bool async)
             {
+                if (BytesWritten != _contentLength)
+                {
+                    return Task.FromException(new HttpRequestException(SR.Format(SR.net_http_request_content_length_mismatch, BytesWritten, _contentLength)));
+                }
+
                 _connection = null;
                 return Task.CompletedTask;
             }
diff --git a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http2Stream.cs b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http2Stream.cs
index b5d5ffa8b84698..3f77cd7f88d61e 100644
--- a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http2Stream.cs
+++ b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/Http2Stream.cs
@@ -195,7 +195,7 @@ public async Task SendRequestBodyAsync(CancellationToken cancellationToken)
 
                     if (sendRequestContent)
                     {
-                        using var writeStream = new Http2WriteStream(this);
+                        using var writeStream = new Http2WriteStream(this, _request.Content.Headers.ContentLength.GetValueOrDefault(-1));
 
                         if (HttpTelemetry.Log.IsEnabled()) HttpTelemetry.Log.RequestContentStart();
 
@@ -214,6 +214,12 @@ public async Task SendRequestBodyAsync(CancellationToken cancellationToken)
                             await vt.ConfigureAwait(false);
                         }
 
+                        if (writeStream.BytesWritten < writeStream.ContentLength)
+                        {
+                            // The number of bytes we actually sent doesn't match the advertised Content-Length
+                            throw new HttpRequestException(SR.Format(SR.net_http_request_content_length_mismatch, writeStream.BytesWritten, writeStream.ContentLength));
+                        }
+
                         if (HttpTelemetry.Log.IsEnabled()) HttpTelemetry.Log.RequestContentStop(writeStream.BytesWritten);
                     }
 
@@ -1506,10 +1512,14 @@ private sealed class Http2WriteStream : HttpBaseStream
 
                 public long BytesWritten { get; private set; }
 
-                public Http2WriteStream(Http2Stream http2Stream)
+                public long ContentLength { get; private set; }
+
+                public Http2WriteStream(Http2Stream http2Stream, long contentLength)
                 {
                     Debug.Assert(http2Stream != null);
+                    Debug.Assert(contentLength >= -1);
                     _http2Stream = http2Stream;
+                    ContentLength = contentLength;
                 }
 
                 protected override void Dispose(bool disposing)
@@ -1534,6 +1544,11 @@ public override ValueTask WriteAsync(ReadOnlyMemory<byte> buffer, CancellationTo
                 {
                     BytesWritten += buffer.Length;
 
+                    if ((ulong)BytesWritten > (ulong)ContentLength) // If ContentLength == -1, this will always be false
+                    {
+                        return ValueTask.FromException(new HttpRequestException(SR.net_http_content_write_larger_than_content_length));
+                    }
+
                     Http2Stream? http2Stream = _http2Stream;
 
                     if (http2Stream == null)
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 e14302ef51f216..357e768e80319e 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
@@ -384,6 +384,14 @@ private async Task SendContentAsync(HttpContent content, CancellationToken cance
                 await content.CopyToAsync(writeStream, null, cancellationToken).ConfigureAwait(false);
             }
 
+            if (_requestContentLengthRemaining > 0)
+            {
+                // The number of bytes we actually sent doesn't match the advertised Content-Length
+                long contentLength = content.Headers.ContentLength.GetValueOrDefault();
+                long sent = contentLength - _requestContentLengthRemaining;
+                throw new HttpRequestException(SR.Format(SR.net_http_request_content_length_mismatch, sent, contentLength));
+            }
+
             // Set to 0 to recognize that the whole request body has been sent and therefore there's no need to abort write side in case of a premature disposal.
             _requestContentLengthRemaining = 0;
 
@@ -414,8 +422,7 @@ private async ValueTask WriteRequestContentAsync(ReadOnlyMemory<byte> buffer, Ca
 
                 if (buffer.Length > _requestContentLengthRemaining)
                 {
-                    string msg = SR.net_http_content_write_larger_than_content_length;
-                    throw new IOException(msg, new HttpRequestException(msg));
+                    throw new HttpRequestException(SR.net_http_content_write_larger_than_content_length);
                 }
                 _requestContentLengthRemaining -= buffer.Length;
 
diff --git a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/HttpConnection.cs b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/HttpConnection.cs
index d75ed2779f0428..12b6b4bf3c55a0 100644
--- a/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/HttpConnection.cs
+++ b/src/libraries/System.Net.Http/src/System/Net/Http/SocketsHttpHandler/HttpConnection.cs
@@ -860,10 +860,11 @@ private bool MapSendException(Exception exception, CancellationToken cancellatio
 
         private HttpContentWriteStream CreateRequestContentStream(HttpRequestMessage request)
         {
+            Debug.Assert(request.Content is not null);
             bool requestTransferEncodingChunked = request.HasHeaders && request.Headers.TransferEncodingChunked == true;
             HttpContentWriteStream requestContentStream = requestTransferEncodingChunked ? (HttpContentWriteStream)
                 new ChunkedEncodingWriteStream(this) :
-                new ContentLengthWriteStream(this);
+                new ContentLengthWriteStream(this, request.Content.Headers.ContentLength.GetValueOrDefault());
             return requestContentStream;
         }
 
diff --git a/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs b/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
index 14f444b1935a60..bd52121a4797b8 100644
--- a/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
+++ b/src/libraries/System.Net.Http/tests/FunctionalTests/SocketsHttpHandlerTest.cs
@@ -3365,4 +3365,70 @@ public sealed class SocketsHttpHandler_RequestValidationTest_Sync : SocketsHttpH
     {
         protected override bool TestAsync => false;
     }
+
+    [ConditionalClass(typeof(PlatformDetection), nameof(PlatformDetection.IsNotBrowser))]
+    public abstract class SocketsHttpHandler_RequestContentLengthMismatchTest : HttpClientHandlerTestBase
+    {
+        public SocketsHttpHandler_RequestContentLengthMismatchTest(ITestOutputHelper output) : base(output) { }
+
+        [Theory]
+        [InlineData(0, 1)]
+        [InlineData(1, 0)]
+        [InlineData(1, 2)]
+        [InlineData(2, 1)]
+        public async Task ContentLength_DoesNotMatchRequestContentLength_Throws(int contentLength, int bytesSent)
+        {
+            await LoopbackServerFactory.CreateClientAndServerAsync(async uri =>
+            {
+                using var client = CreateHttpClient();
+
+                var content = new ByteArrayContent(new byte[bytesSent]);
+                content.Headers.ContentLength = contentLength;
+
+                Exception ex = await Assert.ThrowsAsync<HttpRequestException>(() => client.PostAsync(uri, content));
+                Assert.Contains("Content-Length", ex.Message);
+
+                if (UseVersion.Major == 1)
+                {
+                    await client.GetStringAsync(uri).WaitAsync(TestHelper.PassingTestTimeout);
+                }
+            },
+            async server =>
+            {
+                try
+                {
+                    await server.HandleRequestAsync();
+                }
+                catch { }
+
+                // On HTTP/1.x, an exception being thrown while sending the request content will result in the connection being closed.
+                // This test is ensuring that a subsequent request can succeed on a new connection.
+                if (UseVersion.Major == 1)
+                {
+                    await server.HandleRequestAsync().WaitAsync(TestHelper.PassingTestTimeout);
+                }
+            });
+        }
+    }
+
+    public sealed class SocketsHttpHandler_RequestContentLengthMismatchTest_Http11 : SocketsHttpHandler_RequestContentLengthMismatchTest
+    {
+        public SocketsHttpHandler_RequestContentLengthMismatchTest_Http11(ITestOutputHelper output) : base(output) { }
+        protected override Version UseVersion => HttpVersion.Version11;
+    }
+
+    [ConditionalClass(typeof(PlatformDetection), nameof(PlatformDetection.SupportsAlpn))]
+    public sealed class SocketsHttpHandler_RequestContentLengthMismatchTest_Http2 : SocketsHttpHandler_RequestContentLengthMismatchTest
+    {
+        public SocketsHttpHandler_RequestContentLengthMismatchTest_Http2(ITestOutputHelper output) : base(output) { }
+        protected override Version UseVersion => HttpVersion.Version20;
+    }
+
+    [ConditionalClass(typeof(HttpClientHandlerTestBase), nameof(IsMsQuicSupported))]
+    public sealed class SocketsHttpHandler_RequestContentLengthMismatchTest_Http3 : SocketsHttpHandler_RequestContentLengthMismatchTest
+    {
+        public SocketsHttpHandler_RequestContentLengthMismatchTest_Http3(ITestOutputHelper output) : base(output) { }
+        protected override Version UseVersion => HttpVersion.Version30;
+        protected override QuicImplementationProvider UseQuicImplementationProvider => QuicImplementationProviders.MsQuic;
+    }
 }