diff --git a/src/libraries/System.Net.HttpListener/src/System/Net/Managed/ChunkStream.cs b/src/libraries/System.Net.HttpListener/src/System/Net/Managed/ChunkStream.cs
index d942ce8cca2935..c4daddd7b83d33 100644
--- a/src/libraries/System.Net.HttpListener/src/System/Net/Managed/ChunkStream.cs
+++ b/src/libraries/System.Net.HttpListener/src/System/Net/Managed/ChunkStream.cs
@@ -77,7 +77,6 @@ public int Read(byte[] buffer, int offset, int size)
         private State _state;
         private readonly StringBuilder _saved;
         private bool _sawCR;
-        private bool _gotit;
         private int _trailerState;
         private readonly List<Chunk> _chunks;
 
@@ -150,7 +149,6 @@ private void InternalWrite(byte[] buffer, ref int offset, int size)
 
                 _saved.Length = 0;
                 _sawCR = false;
-                _gotit = false;
             }
 
             if (_state == State.Body && offset < size)
@@ -177,7 +175,6 @@ private void InternalWrite(byte[] buffer, ref int offset, int size)
 
                 _saved.Length = 0;
                 _sawCR = false;
-                _gotit = false;
             }
 
             if (offset < size)
@@ -255,11 +252,7 @@ private State GetChunkSize(byte[] buffer, ref int offset, int size)
                 if (_sawCR && c == '\n')
                     break;
 
-                if (c == ' ')
-                    _gotit = true;
-
-                if (!_gotit)
-                    _saved.Append(c);
+                _saved.Append(c);
 
                 if (_saved.Length > 20)
                     ThrowProtocolViolation("chunk size too long.");
@@ -274,7 +267,7 @@ private State GetChunkSize(byte[] buffer, ref int offset, int size)
                 {
                     if (_saved.Length > 0)
                     {
-                        _chunkSize = int.Parse(RemoveChunkExtension(_saved.ToString()), NumberStyles.HexNumber, CultureInfo.InvariantCulture);
+                        _chunkSize = ParseChunkSize(RemoveChunkExtension(_saved.ToString()));
                     }
                 }
                 catch (Exception)
@@ -288,7 +281,7 @@ private State GetChunkSize(byte[] buffer, ref int offset, int size)
             _chunkRead = 0;
             try
             {
-                _chunkSize = int.Parse(RemoveChunkExtension(_saved.ToString()), NumberStyles.HexNumber, CultureInfo.InvariantCulture);
+                _chunkSize = ParseChunkSize(RemoveChunkExtension(_saved.ToString()));
             }
             catch (Exception)
             {
@@ -310,6 +303,15 @@ private static ReadOnlySpan<char> RemoveChunkExtension(ReadOnlySpan<char> input)
             return idx >= 0 ? input.Slice(0, idx) : input;
         }
 
+        private static int ParseChunkSize(ReadOnlySpan<char> input)
+        {
+            uint chunkSize = uint.Parse(input, NumberStyles.AllowHexSpecifier, CultureInfo.InvariantCulture);
+            if (chunkSize > int.MaxValue)
+                throw new OverflowException();
+
+            return (int)chunkSize;
+        }
+
         private State ReadCRLF(byte[] buffer, ref int offset, int size)
         {
             if (!_sawCR)
diff --git a/src/libraries/System.Net.HttpListener/tests/GetContextHelper.cs b/src/libraries/System.Net.HttpListener/tests/GetContextHelper.cs
index 440f726a333efb..b88e360faf4989 100644
--- a/src/libraries/System.Net.HttpListener/tests/GetContextHelper.cs
+++ b/src/libraries/System.Net.HttpListener/tests/GetContextHelper.cs
@@ -48,7 +48,7 @@ public static class Helpers
         public static bool IsWindowsImplementation { get; } =
             (TypeExists("Interop+HttpApi") || TypeExists("System.Net.UnsafeNclNativeMethods")); // types only in Windows netcoreapp/netfx builds, respectively
 
-        public static bool IsManagedImplementation => TypeExists("System.Net.WebSockets.ManagedWebSocket"); // type only in managed build
+        public static bool IsManagedImplementation => !IsWindowsImplementation;
 
         private static bool TypeExists(string name) => typeof(HttpListener).Assembly.GetType(name, throwOnError: false, ignoreCase: false) != null;
 
diff --git a/src/libraries/System.Net.HttpListener/tests/HttpRequestStreamTests.cs b/src/libraries/System.Net.HttpListener/tests/HttpRequestStreamTests.cs
index 7e5cfdf878a016..2782cfc8bccdd8 100644
--- a/src/libraries/System.Net.HttpListener/tests/HttpRequestStreamTests.cs
+++ b/src/libraries/System.Net.HttpListener/tests/HttpRequestStreamTests.cs
@@ -701,5 +701,66 @@ public async Task Read_FromClosedConnectionSynchronously_ThrowsHttpListenerExcep
                 Assert.Throws<HttpListenerException>(() => context.Request.InputStream.Read(buffer, 0, buffer.Length));
             }
         }
+
+        // http.sys tolerates whitespace around the chunk size and delivers the body, so this
+        // is asserting the behavior of the managed implementation only. Gating on the
+        // implementation rather than the platform keeps it running on Windows when the
+        // managed implementation is force-enabled.
+        [ConditionalTheory(typeof(Helpers), nameof(Helpers.IsManagedImplementation))]
+        [InlineData("5 ")]
+        [InlineData(" 5")]
+        [InlineData(" 5 ")]
+        [InlineData("5\t")]
+        [InlineData("\t5")]
+        [InlineData("5 ;foo=bar")]
+        public async Task Read_ChunkSizeWithWhitespace_ThrowsHttpListenerException(string chunkSizeLine)
+        {
+            using (Socket client = _factory.GetConnectedSocket())
+            {
+                Uri listeningUri = new Uri(_factory.ListeningUrl);
+                string request =
+                    $"POST {listeningUri.PathAndQuery} HTTP/1.1\r\n" +
+                    $"Host: {listeningUri.Host}\r\n" +
+                    "Transfer-Encoding: chunked\r\n" +
+                    "\r\n" +
+                    $"{chunkSizeLine}\r\n" +
+                    "Hello\r\n" +
+                    "0\r\n" +
+                    "\r\n";
+
+                await client.SendAsync(Encoding.ASCII.GetBytes(request));
+                HttpListenerContext context = await _listener.GetContextAsync();
+
+                byte[] buffer = new byte[5];
+                await Assert.ThrowsAsync<HttpListenerException>(() => ReadLengthAsync(context.Request.InputStream, buffer, 0, buffer.Length));
+            }
+        }
+
+        [ConditionalTheory(typeof(Helpers), nameof(Helpers.IsManagedImplementation))]
+        [InlineData("80000000")]
+        [InlineData("FFFFFFFF")]
+        [InlineData("80000000;foo=bar")]
+        public async Task Read_ChunkSizeOverflow_ThrowsHttpListenerException(string chunkSizeLine)
+        {
+            using (Socket client = _factory.GetConnectedSocket())
+            {
+                Uri listeningUri = new Uri(_factory.ListeningUrl);
+                string request =
+                    $"POST {listeningUri.PathAndQuery} HTTP/1.1\r\n" +
+                    $"Host: {listeningUri.Host}\r\n" +
+                    "Transfer-Encoding: chunked\r\n" +
+                    "\r\n" +
+                    $"{chunkSizeLine}\r\n" +
+                    "Hello\r\n" +
+                    "0\r\n" +
+                    "\r\n";
+
+                await client.SendAsync(Encoding.ASCII.GetBytes(request));
+                HttpListenerContext context = await _listener.GetContextAsync();
+
+                byte[] buffer = new byte[5];
+                await Assert.ThrowsAsync<HttpListenerException>(() => ReadLengthAsync(context.Request.InputStream, buffer, 0, buffer.Length));
+            }
+        }
     }
 }