diff --git a/cli/tests/unit/http_test.ts b/cli/tests/unit/http_test.ts
index ab43323bd4..d4c35545f5 100644
--- a/cli/tests/unit/http_test.ts
+++ b/cli/tests/unit/http_test.ts
@@ -272,3 +272,48 @@ unitTest(
     await promise;
   },
 );
+
+unitTest(
+  { perms: { net: true } },
+  async function httpServerNextRequestErrorExposedInResponse() {
+    const promise = (async () => {
+      const listener = Deno.listen({ port: 4501 });
+      const conn = await listener.accept();
+      const httpConn = Deno.serveHttp(conn);
+      const event = await httpConn.nextRequest();
+      assert(event);
+      // Start polling for the next request before awaiting response.
+      const nextRequestPromise = httpConn.nextRequest();
+      const { respondWith } = event;
+      await assertThrowsAsync(
+        async () => {
+          let interval = 0;
+          await respondWith(
+            new Response(
+              new ReadableStream({
+                start(controller) {
+                  interval = setInterval(() => {
+                    const message = `data: ${Date.now()}\n\n`;
+                    controller.enqueue(new TextEncoder().encode(message));
+                  }, 200);
+                },
+                cancel() {
+                  clearInterval(interval);
+                },
+              }),
+            ),
+          );
+        },
+        Deno.errors.Http,
+        "connection closed",
+      );
+      // The error from `op_http_request_next` reroutes to `respondWith()`.
+      assertEquals(await nextRequestPromise, null);
+      listener.close();
+    })();
+
+    const resp = await fetch("http://127.0.0.1:4501/");
+    await resp.body!.cancel();
+    await promise;
+  },
+);
diff --git a/runtime/js/40_http.js b/runtime/js/40_http.js
index eb3c58a632..eb4d214ca4 100644
--- a/runtime/js/40_http.js
+++ b/runtime/js/40_http.js
@@ -14,6 +14,8 @@
     return new HttpConn(rid);
   }
 
+  const connErrorSymbol = Symbol("connError");
+
   class HttpConn {
     #rid = 0;
 
@@ -35,10 +37,16 @@
           this.#rid,
         );
       } catch (error) {
+        // A connection error seen here would cause disrupted responses to throw
+        // a generic `BadResource` error. Instead store this error and replace
+        // those with it.
+        this[connErrorSymbol] = error;
         if (error instanceof errors.BadResource) {
           return null;
         } else if (error instanceof errors.Interrupted) {
           return null;
+        } else if (error.message.includes("connection closed")) {
+          return null;
         }
         throw error;
       }
@@ -66,7 +74,7 @@
       );
       const request = fromInnerRequest(innerRequest, "immutable");
 
-      const respondWith = createRespondWith(responseSenderRid, this.#rid);
+      const respondWith = createRespondWith(this, responseSenderRid);
 
       return { request, respondWith };
     }
@@ -97,7 +105,7 @@
     );
   }
 
-  function createRespondWith(responseSenderRid) {
+  function createRespondWith(httpConn, responseSenderRid) {
     return async function respondWith(resp) {
       if (resp instanceof Promise) {
         resp = await resp;
@@ -145,6 +153,11 @@
           innerResp.headerList,
         ], respBody instanceof Uint8Array ? respBody : null);
       } catch (error) {
+        const connError = httpConn[connErrorSymbol];
+        if (error instanceof errors.BadResource && connError != null) {
+          // deno-lint-ignore no-ex-assign
+          error = new connError.constructor(connError.message);
+        }
         if (respBody !== null && respBody instanceof ReadableStream) {
           await respBody.cancel(error);
         }
@@ -173,6 +186,11 @@
                 value,
               );
             } catch (error) {
+              const connError = httpConn[connErrorSymbol];
+              if (error instanceof errors.BadResource && connError != null) {
+                // deno-lint-ignore no-ex-assign
+                error = new connError.constructor(connError.message);
+              }
               await reader.cancel(error);
               throw error;
             }
@@ -180,7 +198,9 @@
         } finally {
           // Once all chunks are sent, and the request body is closed, we can
           // close the response body.
-          await Deno.core.opAsync("op_http_response_close", responseBodyRid);
+          try {
+            await Deno.core.opAsync("op_http_response_close", responseBodyRid);
+          } catch { /* pass */ }
         }
       }
     };