diff --git a/cli/tests/unit/http_test.ts b/cli/tests/unit/http_test.ts
index 9560394f04..df599c6f4f 100644
--- a/cli/tests/unit/http_test.ts
+++ b/cli/tests/unit/http_test.ts
@@ -339,3 +339,37 @@ unitTest(
     await promise;
   },
 );
+
+unitTest(
+  { perms: { net: true } },
+  async function httpServerNextRequestResolvesOnClose() {
+    const delay = (n: number) =>
+      new Promise((resolve) => setTimeout(resolve, n));
+    const httpConnList: Deno.HttpConn[] = [];
+
+    async function serve(l: Deno.Listener) {
+      for await (const conn of l) {
+        (async () => {
+          const c = Deno.serveHttp(conn);
+          httpConnList.push(c);
+          for await (const { respondWith } of c) {
+            respondWith(new Response("hello"));
+          }
+        })();
+      }
+    }
+
+    const l = Deno.listen({ port: 4500 });
+    serve(l);
+
+    await delay(300);
+    const res = await fetch("http://localhost:4500/");
+    const _text = await res.text();
+
+    // Close connection and listener.
+    httpConnList.forEach((conn) => conn.close());
+    l.close();
+
+    await delay(300);
+  },
+);
diff --git a/runtime/ops/http.rs b/runtime/ops/http.rs
index e4ba2db2a5..fedcb404f5 100644
--- a/runtime/ops/http.rs
+++ b/runtime/ops/http.rs
@@ -14,7 +14,6 @@ use deno_core::futures::StreamExt;
 use deno_core::op_async;
 use deno_core::op_sync;
 use deno_core::AsyncRefCell;
-use deno_core::CancelFuture;
 use deno_core::CancelHandle;
 use deno_core::CancelTryFuture;
 use deno_core::Extension;
@@ -107,6 +106,7 @@ struct ConnResource {
   hyper_connection: ConnType,
   deno_service: Service,
   addr: SocketAddr,
+  cancel: CancelHandle,
 }
 
 impl ConnResource {
@@ -124,6 +124,10 @@ impl Resource for ConnResource {
   fn name(&self) -> Cow<str> {
     "httpConnection".into()
   }
+
+  fn close(self: Rc<Self>) {
+    self.cancel.cancel()
+  }
 }
 
 // We use a tuple instead of struct to avoid serialization overhead of the keys.
@@ -153,6 +157,8 @@ async fn op_http_request_next(
     .get::<ConnResource>(conn_rid)
     .ok_or_else(bad_resource_id)?;
 
+  let cancel = RcRef::map(conn_resource.clone(), |r| &r.cancel);
+
   poll_fn(|cx| {
     let connection_closed = match conn_resource.poll(cx) {
       Poll::Pending => false,
@@ -257,6 +263,7 @@ async fn op_http_request_next(
       Poll::Pending
     }
   })
+  .try_or_cancel(cancel)
   .await
   .map_err(AnyError::from)
 }
@@ -298,6 +305,7 @@ fn op_http_start(
       hyper_connection: ConnType::Tcp(Rc::new(RefCell::new(hyper_connection))),
       deno_service,
       addr,
+      cancel: CancelHandle::default(),
     };
     let rid = state.resource_table.add(conn_resource);
     return Ok(rid);
@@ -320,6 +328,7 @@ fn op_http_start(
       hyper_connection: ConnType::Tls(Rc::new(RefCell::new(hyper_connection))),
       deno_service,
       addr,
+      cancel: CancelHandle::default(),
     };
     let rid = state.resource_table.add(conn_resource);
     return Ok(rid);
@@ -381,7 +390,6 @@ async fn op_http_response(
     let response_body_rid =
       state.borrow_mut().resource_table.add(ResponseBodyResource {
         body: AsyncRefCell::new(sender),
-        cancel: CancelHandle::default(),
         conn_rid: response_sender.conn_rid,
       });
 
@@ -484,12 +492,8 @@ async fn op_http_response_write(
     .ok_or_else(bad_resource_id)?;
 
   let mut body = RcRef::map(&resource, |r| &r.body).borrow_mut().await;
-  let cancel = RcRef::map(resource, |r| &r.cancel);
 
-  let mut send_data_fut = body
-    .send_data(Vec::from(&*buf).into())
-    .or_cancel(cancel)
-    .boxed_local();
+  let mut send_data_fut = body.send_data(Vec::from(&*buf).into()).boxed_local();
 
   poll_fn(|cx| {
     if let Poll::Ready(Err(e)) = conn_resource.poll(cx) {
@@ -501,8 +505,7 @@ async fn op_http_response_write(
 
     send_data_fut.poll_unpin(cx).map_err(AnyError::from)
   })
-  .await?
-  .unwrap(); // panic on send_data error
+  .await?;
 
   Ok(())
 }
@@ -520,6 +523,10 @@ impl Resource for RequestBodyResource {
   fn name(&self) -> Cow<str> {
     "requestBody".into()
   }
+
+  fn close(self: Rc<Self>) {
+    self.cancel.cancel()
+  }
 }
 
 struct ResponseSenderResource {
@@ -535,7 +542,6 @@ impl Resource for ResponseSenderResource {
 
 struct ResponseBodyResource {
   body: AsyncRefCell<hyper::body::Sender>,
-  cancel: CancelHandle,
   conn_rid: ResourceId,
 }