diff --git a/src/jsc/SystemError.rs b/src/jsc/SystemError.rs
index b2fd3c3b13df..2ff6e2d3bffa 100644
--- a/src/jsc/SystemError.rs
+++ b/src/jsc/SystemError.rs
@@ -8,6 +8,7 @@ use crate::{JSGlobalObject, JSPromise, JSValue};
 #[repr(C)]
 #[derive(Clone)]
 pub struct SystemError {
+    /// [`SystemError::NO_ERRNO`] = the JS error gets `errno: undefined`
     pub errno: c_int,
     /// label for errno
     pub code: OwnedString,
@@ -80,6 +81,12 @@ unsafe extern "C" {
 }
 
 impl SystemError {
+    /// `errno` for an error that has no numeric system error code, only a
+    /// string `code`. Node reports such errors (a c-ares resolver failure, for
+    /// example) with an own `errno` property whose value is `undefined`, and
+    /// the C++ side (`systemErrorToErrorInstance`) emits exactly that.
+    pub const NO_ERRNO: c_int = c_int::MIN;
+
     /// Converts to a JS `Error`, consuming `self`. C++ only borrows the string
     /// fields; `Drop` releases them when `self` goes out of scope. `.clone()`
     /// first when two `Error`s are genuinely wanted.
diff --git a/src/jsc/bindings/bindings.cpp b/src/jsc/bindings/bindings.cpp
index 147f9a5ec434..293da5cf2b57 100644
--- a/src/jsc/bindings/bindings.cpp
+++ b/src/jsc/bindings/bindings.cpp
@@ -2569,6 +2569,15 @@ JSC::EncodedJSValue JSGlobalObject__createOutOfMemoryError(JSC::JSGlobalObject*
     return JSValue::encode(exception);
 }
 
+// `SystemError::NO_ERRNO` on the Rust side: the error has a string `code` but
+// no numeric errno, and Node reports those with `errno: undefined`.
+static JSC::JSValue systemErrorErrnoValue(const SystemError& err)
+{
+    if (err.errno_ == std::numeric_limits<int>::min())
+        return JSC::jsUndefined();
+    return JSC::jsNumber(err.errno_);
+}
+
 static JSC::EncodedJSValue systemErrorToErrorInstance(const SystemError* arg0, JSC::JSGlobalObject* globalObject, JSC::ErrorType errorType)
 {
     SystemError err = *arg0;
@@ -2637,7 +2646,7 @@ static JSC::EncodedJSValue systemErrorToErrorInstance(const SystemError* arg0, J
         }
     }
 
-    result->putDirect(vm, names.errnoPublicName(), jsNumber(err.errno_), JSC::PropertyAttribute::DontDelete | 0);
+    result->putDirect(vm, names.errnoPublicName(), systemErrorErrnoValue(err), JSC::PropertyAttribute::DontDelete | 0);
 
     return JSC::JSValue::encode(result);
 }
@@ -2683,8 +2692,9 @@ JSC::EncodedJSValue SystemError__toErrorInstanceWithInfoObject(const SystemError
     info->putDirect(vm, clientData->builtinNames().codePublicName(), jsString(vm, codeString), JSC::PropertyAttribute::DontDelete | 0);
     info->putDirect(vm, vm.propertyNames->message, jsString(vm, messageString), JSC::PropertyAttribute::DontDelete | 0);
 
-    info->putDirect(vm, clientData->builtinNames().errnoPublicName(), jsNumber(err.errno_), JSC::PropertyAttribute::DontDelete | 0);
-    result->putDirect(vm, clientData->builtinNames().errnoPublicName(), jsNumber(err.errno_), JSC::PropertyAttribute::DontDelete | 0);
+    JSC::JSValue errnoValue = systemErrorErrnoValue(err);
+    info->putDirect(vm, clientData->builtinNames().errnoPublicName(), errnoValue, JSC::PropertyAttribute::DontDelete | 0);
+    result->putDirect(vm, clientData->builtinNames().errnoPublicName(), errnoValue, JSC::PropertyAttribute::DontDelete | 0);
 
     return JSC::JSValue::encode(result);
 }
diff --git a/src/jsc/bindings/headers-handwritten.h b/src/jsc/bindings/headers-handwritten.h
index 699d909ad7fd..f4a7f036f9d7 100644
--- a/src/jsc/bindings/headers-handwritten.h
+++ b/src/jsc/bindings/headers-handwritten.h
@@ -144,6 +144,7 @@ typedef struct ErrorableResolvedSource {
 } ErrorableResolvedSource;
 
 typedef struct SystemError {
+    /// MinInt (`SystemError::NO_ERRNO` in Rust) = the error gets `errno: undefined`
     int errno_;
     BunString code;
     BunString message;
diff --git a/src/runtime/dns_jsc/cares_jsc.rs b/src/runtime/dns_jsc/cares_jsc.rs
index 7492e72296e9..5beddf1441fd 100644
--- a/src/runtime/dns_jsc/cares_jsc.rs
+++ b/src/runtime/dns_jsc/cares_jsc.rs
@@ -640,6 +640,18 @@ fn any_reply_to_js(
 }
 
 // ── Error ──────────────────────────────────────────────────────────────────
+
+/// Node only gives a DNS error a numeric `errno` when libuv reported one
+/// (`getaddrinfo`/`getnameinfo`). A c-ares resolver failure (`query*`,
+/// `getHostByAddr`) only has a string `code`, so its `errno` is undefined.
+fn errno_for_syscall(this: c_ares::Error, syscall: &[u8]) -> c_int {
+    if strings::has_prefix_comptime(syscall, b"query") || strings::eql(syscall, b"getHostByAddr") {
+        SystemError::NO_ERRNO
+    } else {
+        this as c_int
+    }
+}
+
 pub(crate) struct ErrorDeferred {
     pub errno: c_ares::Error,
     pub syscall: &'static [u8],
@@ -679,7 +691,7 @@ impl ErrorDeferred {
             ))
         };
         let system_error = SystemError {
-            errno: self.errno as i32,
+            errno: errno_for_syscall(self.errno, self.syscall),
             code: bstr::String::static_(code).into(),
             message: message.into(),
             syscall: bstr::String::clone_utf8(self.syscall).into(),
@@ -765,7 +777,7 @@ pub(crate) fn error_to_js_with_syscall(
 ) -> JsResult<JSValue> {
     let code = this.code();
     let instance = SystemError {
-        errno: this as i32,
+        errno: errno_for_syscall(this, syscall),
         code: bstr::String::static_(&code[4..]).into(),
         syscall: bstr::String::static_(syscall).into(),
         message: bstr::String::create_format(format_args!(
@@ -797,7 +809,7 @@ pub(crate) fn system_error_with_syscall_and_hostname(
 ) -> SystemError {
     let code = this.code();
     SystemError {
-        errno: this as i32,
+        errno: errno_for_syscall(this, syscall),
         code: bstr::String::static_(&code[4..]).into(),
         message: bstr::String::create_format(format_args!(
             "{} {} {}",
diff --git a/test/js/node/dns/node-dns.test.js b/test/js/node/dns/node-dns.test.js
index 0e0853c216c6..1bf8e42fad7c 100644
--- a/test/js/node/dns/node-dns.test.js
+++ b/test/js/node/dns/node-dns.test.js
@@ -157,6 +157,101 @@ test.skipIf(isWindows)("dns.resolveSrv accepts compressed target in RDATA", asyn
   }
 });
 
+// Node only sets a numeric `errno` on DNS errors when libuv reported a
+// numeric error (getaddrinfo/getnameinfo). c-ares resolver failures carry a
+// string code and leave `errno` undefined. https://github.com/oven-sh/bun/issues/37320
+test.skipIf(isWindows)("resolver query errors leave errno undefined, lookup errors keep a number", async () => {
+  const socket = dgram.createSocket("udp4");
+  try {
+    socket.on("message", (query, rinfo) => {
+      // Reply NXDOMAIN to every query.
+      const res = Buffer.from(query);
+      res[2] = 0x81; // QR=1, RD=1
+      res[3] = 0x83; // RA=1, RCODE=3 (NXDOMAIN)
+      res.fill(0, 6, 12); // ANCOUNT/NSCOUNT/ARCOUNT = 0
+      socket.send(res, rinfo.port, rinfo.address);
+    });
+    socket.bind(0, "127.0.0.1");
+    await once(socket, "listening");
+    const { port } = socket.address();
+
+    const servers = ["127.0.0.1:" + port];
+    const resolver = new dns.Resolver({ timeout: 1000, tries: 1 });
+    resolver.setServers(servers);
+    const promisesResolver = new dns.promises.Resolver({ timeout: 1000, tries: 1 });
+    promisesResolver.setServers(servers);
+
+    const unexpectedSuccess = new Error("expected the query to fail");
+    const callbackError = query =>
+      new Promise((resolve, reject) => query(err => (err ? resolve(err) : reject(unexpectedSuccess))));
+    const promiseError = promise =>
+      promise.then(
+        () => {
+          throw unexpectedSuccess;
+        },
+        err => err,
+      );
+
+    const errors = {
+      resolve4: await callbackError(cb => resolver.resolve4("invalid.invalid", cb)),
+      resolveAny: await callbackError(cb => resolver.resolveAny("invalid.invalid", cb)),
+      reverse: await callbackError(cb => resolver.reverse("192.0.2.1", cb)),
+      promisesResolve4: await promiseError(promisesResolver.resolve4("invalid.invalid")),
+      promisesResolveAny: await promiseError(promisesResolver.resolveAny("invalid.invalid")),
+      promisesReverse: await promiseError(promisesResolver.reverse("192.0.2.1")),
+      // dns.lookup() rejects a name with a NUL byte before it reaches a resolver
+      // backend, so this getaddrinfo failure does not need the network either.
+      lookup: await promiseError(dns.promises.lookup("invalid.invalid\0")),
+    };
+
+    // Node keeps `errno` as an own property of the error and only leaves its
+    // value undefined, so check the property is still there.
+    const shapes = Object.fromEntries(
+      Object.entries(errors).map(([name, err]) => [
+        name,
+        {
+          code: err.code,
+          syscall: err.syscall,
+          hostname: err.hostname,
+          errno: err.errno,
+          hasOwnErrno: Object.hasOwn(err, "errno"),
+        },
+      ]),
+    );
+    const query = syscall => ({
+      code: "ENOTFOUND",
+      syscall,
+      hostname: "invalid.invalid",
+      errno: undefined,
+      hasOwnErrno: true,
+    });
+    const reverse = {
+      code: "ENOTFOUND",
+      syscall: "getHostByAddr",
+      hostname: "192.0.2.1",
+      errno: undefined,
+      hasOwnErrno: true,
+    };
+    expect(shapes).toEqual({
+      resolve4: query("queryA"),
+      resolveAny: query("queryAny"),
+      reverse,
+      promisesResolve4: query("queryA"),
+      promisesResolveAny: query("queryAny"),
+      promisesReverse: reverse,
+      lookup: {
+        code: "ENOTFOUND",
+        syscall: "getaddrinfo",
+        hostname: "invalid.invalid\0",
+        errno: expect.any(Number),
+        hasOwnErrno: true,
+      },
+    });
+  } finally {
+    socket.close();
+  }
+});
+
 test("dns.resolveTxt (txt.socketify.dev)", () => {
   const { promise, resolve, reject } = Promise.withResolvers();
   dns.resolveTxt("txt.socketify.dev", (err, results) => {
@@ -404,6 +499,8 @@ test("dns.lookup bad (qedjp3f4q4jgjh4d6vaf3fd2hbfhg6upt2bscrfe.com)", () => {
       expect(err).not.toBeNull();
       expect(err.syscall).toEqual("getaddrinfo");
       expect(err.code).toEqual("ENOTFOUND");
+      // Unlike resolver query errors, lookup errors keep a numeric errno in Node.
+      expect(err.errno).toBeNumber();
       expect(address).toBeUndefined();
       expect(family).toBeUndefined();
       resolve();