diff --git a/src/jsifier.mjs b/src/jsifier.mjs
index dbe20035574e1..84fe9d01b129a 100644
--- a/src/jsifier.mjs
+++ b/src/jsifier.mjs
@@ -360,16 +360,29 @@ ${body};
   });
 }
 
-function handleAsyncFunction(snippet, sig) {
+function handleAsyncFunction(snippet, sig, proxyingMode) {
   const return64 = sig && (MEMORY64 && sig.startsWith('p') || sig.startsWith('j'))
   let handleAsync = 'Asyncify.handleAsync(innerFunc)'
   if (return64 && ASYNCIFY == 1) {
     handleAsync = makeReturn64(handleAsync);
   }
+  // When a function uses both __proxy:'sync' and __async:'auto', the proxy
+  // mechanism (PROXY_SYNC_ASYNC) handles the async return itself.  In that
+  // case, skip the Asyncify unwind and call the inner function directly so
+  // the proxy can use .then() on the returned Promise.
+  const skipHandleAsync = PTHREADS && ASYNCIFY == 1 && proxyingMode === 'sync';
   return modifyJSFunction(snippet, (args, body, async_, oneliner) => {
     if (!oneliner) {
       body = `{\n${body}\n}`;
     }
+    if (skipHandleAsync) {
+      return `\
+function(${args}) {
+  let innerFunc = async () => ${body};
+  if (PThread.currentProxiedOperationCallerThread) return innerFunc();
+  return ${handleAsync};
+}\n`;
+    }
     return `\
 function(${args}) {
   let innerFunc = ${async_} () => ${body};
@@ -474,11 +487,11 @@ function(${args}) {
       compileTimeContext.i53ConversionDeps.forEach((d) => deps.push(d));
     }
 
+    const proxyingMode = LibraryManager.library[symbol + '__proxy'];
+
     if (ASYNCIFY && isAsyncFunction == 'auto') {
-      snippet = handleAsyncFunction(snippet, sig);
+      snippet = handleAsyncFunction(snippet, sig, proxyingMode);
     }
-
-    const proxyingMode = LibraryManager.library[symbol + '__proxy'];
     if (proxyingMode) {
       if (!['sync', 'async', 'none'].includes(proxyingMode)) {
         error(`JS library error: invalid proxying mode '${symbol}__proxy: ${proxyingMode}' specified`);
diff --git a/test/test_core.py b/test/test_core.py
index 7f2766fb1464e..668aaa156380e 100644
--- a/test/test_core.py
+++ b/test/test_core.py
@@ -9645,6 +9645,18 @@ def test_poll_blocking_asyncify(self):
       self.skipTest('test requires setTimeout which is not supported under v8')
     self.do_runf('core/test_poll_blocking_asyncify.c', 'done\n')
 
+  @no_esm_integration('WASM_ESM_INTEGRATION is not compatible with ASYNCIFY=1')
+  @requires_pthreads
+  def test_poll_blocking_asyncify_pthread(self):
+    # Only testing ASYNCIFY=1: JSPI's handleAsync is a plain async function
+    # and doesn't have this bug.  Also, with_asyncify_and_jspi can't be
+    # combined with requires_pthreads since require_jspi may select d8 which
+    # doesn't support pthreads (require_pthreads then hard-fails instead of
+    # skipping).
+    self.set_setting('ASYNCIFY')
+    self.do_runf('core/test_poll_blocking.c', 'done\n',
+                 cflags=['-sPROXY_TO_PTHREAD', '-sEXIT_RUNTIME'])
+
   @parameterized({
     '': ([],),
     'pthread': (['-pthread'],),