diff --git a/cli/tests/unit/serve_test.ts b/cli/tests/unit/serve_test.ts
index 2e7836b6a9..830817146a 100644
--- a/cli/tests/unit/serve_test.ts
+++ b/cli/tests/unit/serve_test.ts
@@ -2699,12 +2699,14 @@ Deno.test(
 
 for (const url of ["text", "file", "stream"]) {
   // Ensure that we don't panic when the incoming TCP request was dropped
-  // https://github.com/denoland/deno/issues/20315
+  // https://github.com/denoland/deno/issues/20315 and that we correctly
+  // close/cancel the response
   Deno.test({
     permissions: { read: true, write: true, net: true },
     name: `httpServerTcpCancellation_${url}`,
     fn: async function () {
       const ac = new AbortController();
+      const streamCancelled = url == "stream" ? deferred() : undefined;
       const listeningPromise = deferred();
       const waitForAbort = deferred();
       const waitForRequest = deferred();
@@ -2727,7 +2729,9 @@ for (const url of ["text", "file", "stream"]) {
                 start(controller) {
                   _body = null;
                   controller.enqueue(new Uint8Array([1]));
-                  controller.close();
+                },
+                cancel(reason) {
+                  streamCancelled!.resolve(reason);
                 },
               }),
             );
@@ -2753,14 +2757,56 @@ for (const url of ["text", "file", "stream"]) {
       // Give it a few milliseconds for the serve machinery to work
       await new Promise((r) => setTimeout(r, 10));
 
+      // Wait for cancellation before we shut the server down
+      if (streamCancelled !== undefined) {
+        await streamCancelled;
+      }
+
       // Since the handler has a chance of creating resources or running async ops, we need to use a
       // graceful shutdown here to ensure they have fully drained.
       await server.shutdown();
+
       await server.finished;
     },
   });
 }
 
+Deno.test(
+  { permissions: { net: true } },
+  async function httpServerCancelFetch() {
+    const request2 = deferred();
+    const request2Aborted = deferred();
+    const { finished, abort } = await makeServer(async (req) => {
+      if (req.url.endsWith("/1")) {
+        const fetchRecursive = await fetch(`http://localhost:${servePort}/2`);
+        return new Response(fetchRecursive.body);
+      } else if (req.url.endsWith("/2")) {
+        request2.resolve();
+        return new Response(
+          new ReadableStream({
+            start(_controller) {/* just hang */},
+            cancel(reason) {
+              request2Aborted.resolve(reason);
+            },
+          }),
+        );
+      }
+      fail();
+    });
+    const fetchAbort = new AbortController();
+    const fetchPromise = await fetch(`http://localhost:${servePort}/1`, {
+      signal: fetchAbort.signal,
+    });
+    await fetchPromise;
+    await request2;
+    fetchAbort.abort();
+    assertEquals("resource closed", await request2Aborted);
+
+    abort();
+    await finished;
+  },
+);
+
 Deno.test(
   { permissions: { read: true, net: true } },
   async function httpServerWithTls() {
diff --git a/ext/http/http_next.rs b/ext/http/http_next.rs
index 21e138f860..7ccd9ec816 100644
--- a/ext/http/http_next.rs
+++ b/ext/http/http_next.rs
@@ -577,10 +577,13 @@ fn ensure_vary_accept_encoding(hmap: &mut HeaderMap) {
   );
 }
 
+/// Sets the appropriate response body. Use `force_instantiate_body` if you need
+/// to ensure that the response is cleaned up correctly (eg: for resources).
 fn set_response(
   slab_id: SlabId,
   length: Option<usize>,
   status: u16,
+  force_instantiate_body: bool,
   response_fn: impl FnOnce(Compression) -> ResponseBytesInner,
 ) {
   let mut http = slab_get(slab_id);
@@ -602,7 +605,10 @@ fn set_response(
     if let Ok(code) = StatusCode::from_u16(status) {
       *response.status_mut() = code;
     }
+  } else if force_instantiate_body {
+    response_fn(Compression::None).abort();
   }
+
   http.complete();
 }
 
@@ -634,6 +640,7 @@ pub fn op_http_set_response_body_resource(
     slab_id,
     resource.size_hint().1.map(|s| s as usize),
     status,
+    true,
     move |compression| {
       ResponseBytesInner::from_resource(compression, resource, auto_close)
     },
@@ -649,7 +656,7 @@ pub fn op_http_set_response_body_text(
   status: u16,
 ) {
   if !text.is_empty() {
-    set_response(slab_id, Some(text.len()), status, |compression| {
+    set_response(slab_id, Some(text.len()), status, false, |compression| {
       ResponseBytesInner::from_vec(compression, text.into_bytes())
     });
   } else {
@@ -665,7 +672,7 @@ pub fn op_http_set_response_body_bytes(
   status: u16,
 ) {
   if !buffer.is_empty() {
-    set_response(slab_id, Some(buffer.len()), status, |compression| {
+    set_response(slab_id, Some(buffer.len()), status, false, |compression| {
       ResponseBytesInner::from_bufview(compression, BufView::from(buffer))
     });
   } else {
diff --git a/ext/http/response_body.rs b/ext/http/response_body.rs
index 5c946a4d3c..4f7e3b0a5d 100644
--- a/ext/http/response_body.rs
+++ b/ext/http/response_body.rs
@@ -125,6 +125,16 @@ pub enum ResponseStream {
   TestChannel(tokio::sync::mpsc::Receiver<BufView>),
 }
 
+impl ResponseStream {
+  pub fn abort(self) {
+    match self {
+      ResponseStream::Resource(resource) => resource.stm.close(),
+      #[cfg(test)]
+      ResponseStream::TestChannel(..) => {}
+    }
+  }
+}
+
 #[derive(Default)]
 pub enum ResponseBytesInner {
   /// An empty stream.
@@ -192,11 +202,25 @@ impl ResponseBytes {
 
     let current = std::mem::replace(&mut self.inner, ResponseBytesInner::Done);
     self.completion_handle.complete(success);
-    current
+    if success {
+      current
+    } else {
+      current.abort();
+      ResponseBytesInner::Done
+    }
   }
 }
 
 impl ResponseBytesInner {
+  pub fn abort(self) {
+    match self {
+      Self::Done | Self::Empty | Self::Bytes(..) => {}
+      Self::BrotliStream(stm) => stm.abort(),
+      Self::GZipStream(stm) => stm.abort(),
+      Self::UncompressedStream(stm) => stm.abort(),
+    }
+  }
+
   pub fn size_hint(&self) -> SizeHint {
     match self {
       Self::Done => SizeHint::with_exact(0),
@@ -463,6 +487,10 @@ impl GZipResponseStream {
       underlying,
     }
   }
+
+  pub fn abort(self) {
+    self.underlying.abort()
+  }
 }
 
 /// This is a minimal GZip header suitable for serving data from a webserver. We don't need to provide
@@ -645,6 +673,10 @@ impl BrotliResponseStream {
       underlying,
     }
   }
+
+  pub fn abort(self) {
+    self.underlying.abort()
+  }
 }
 
 fn max_compressed_size(input_size: usize) -> usize {
diff --git a/ext/web/stream_resource.rs b/ext/web/stream_resource.rs
index e19954fdca..b35d4c302d 100644
--- a/ext/web/stream_resource.rs
+++ b/ext/web/stream_resource.rs
@@ -364,6 +364,15 @@ impl ReadableStreamResource {
       .read(limit)
       .map(|buf| buf.unwrap_or_else(BufView::empty))
   }
+
+  fn close_channel(&self) {
+    // Trigger the promise in JS to cancel the stream if necessarily
+    self.data.completion.complete(true);
+    // Cancel any outstanding read requests
+    self.cancel_handle.cancel();
+    // Close the channel to wake up anyone waiting
+    self.channel.close();
+  }
 }
 
 impl Resource for ReadableStreamResource {
@@ -376,8 +385,13 @@ impl Resource for ReadableStreamResource {
   }
 
   fn close(self: Rc<Self>) {
-    self.cancel_handle.cancel();
-    self.channel.close();
+    self.close_channel();
+  }
+}
+
+impl Drop for ReadableStreamResource {
+  fn drop(&mut self) {
+    self.close_channel();
   }
 }