diff --git a/.changeset/few-planets-attend.md b/.changeset/few-planets-attend.md
new file mode 100644
index 00000000000..1777c4cd74f
--- /dev/null
+++ b/.changeset/few-planets-attend.md
@@ -0,0 +1,5 @@
+---
+"@remix-run/architect": patch
+---
+
+Manually joining headers with semi-colons to avoid differences in Remix and node/undici Headers implementation.
diff --git a/contributors.yml b/contributors.yml
index a1c32df2763..9317d74d7ce 100644
--- a/contributors.yml
+++ b/contributors.yml
@@ -114,6 +114,7 @@
 - colinhacks
 - confix
 - coryhouse
+- courey
 - courtyenn
 - craigayre
 - craigglennie
diff --git a/packages/remix-architect/__tests__/server-test.ts b/packages/remix-architect/__tests__/server-test.ts
index 196f00f9488..243ff5ad99c 100644
--- a/packages/remix-architect/__tests__/server-test.ts
+++ b/packages/remix-architect/__tests__/server-test.ts
@@ -1,6 +1,7 @@
 import fsp from "node:fs/promises";
 import path from "node:path";
 import { createRequestHandler as createRemixRequestHandler } from "@remix-run/node";
+import { Headers as RemixHeaders } from "@remix-run/web-fetch";
 import type { APIGatewayProxyEventV2 } from "aws-lambda";
 import lambdaTester from "lambda-tester";
 
@@ -230,6 +231,18 @@ describe("architect createRemixHeaders", () => {
         "__session=some_value; __other=some_other_value"
       );
     });
+
+    it("handles multiple request cookies when using @remix-run/web-fetch", () => {
+      let headers = createRemixHeaders(
+        {},
+        ["__session=some_value", "__other=some_other_value"],
+        // @ts-expect-error types don't align since it's not fully spec compliant
+        RemixHeaders
+      );
+      expect(headers.get("cookie")).toEqual(
+        "__session=some_value; __other=some_other_value"
+      );
+    });
   });
 });
 
diff --git a/packages/remix-architect/package.json b/packages/remix-architect/package.json
index e008402bcdd..dcfdffaf0b1 100644
--- a/packages/remix-architect/package.json
+++ b/packages/remix-architect/package.json
@@ -19,6 +19,7 @@
   "dependencies": {
     "@architect/functions": "^5.2.0",
     "@remix-run/node": "workspace:*",
+    "@remix-run/web-fetch": "^4.4.2",
     "@types/aws-lambda": "^8.10.82"
   },
   "devDependencies": {
diff --git a/packages/remix-architect/server.ts b/packages/remix-architect/server.ts
index 6ad6c1c692b..52fa5a0bcd3 100644
--- a/packages/remix-architect/server.ts
+++ b/packages/remix-architect/server.ts
@@ -77,9 +77,15 @@ export function createRemixRequest(event: APIGatewayProxyEventV2): Request {
 
 export function createRemixHeaders(
   requestHeaders: APIGatewayProxyEventHeaders,
-  requestCookies?: string[]
+  requestCookies?: string[],
+  _Headers?: typeof Headers
 ): Headers {
-  let headers = new Headers();
+  // `_Headers` should only be used for unit testing purposes so we can unit test
+  // the different behaviors of the @remix-run/web-fetch `Headers` implementation
+  // and the node/undici implementation.  See:
+  // https://github.com/remix-run/remix/issues/9657
+  let HeadersImpl = _Headers || Headers;
+  let headers = new HeadersImpl();
 
   for (let [header, value] of Object.entries(requestHeaders)) {
     if (value) {
@@ -88,9 +94,7 @@ export function createRemixHeaders(
   }
 
   if (requestCookies) {
-    for (let cookie of requestCookies) {
-      headers.append("Cookie", cookie);
-    }
+    headers.append("Cookie", requestCookies.join("; "));
   }
 
   return headers;
diff --git a/pnpm-lock.yaml b/pnpm-lock.yaml
index e62b78bd283..65b97bab3a0 100644
--- a/pnpm-lock.yaml
+++ b/pnpm-lock.yaml
@@ -744,6 +744,9 @@ importers:
       '@remix-run/node':
         specifier: workspace:*
         version: link:../remix-node
+      '@remix-run/web-fetch':
+        specifier: ^4.4.2
+        version: 4.4.2
       '@types/aws-lambda':
         specifier: ^8.10.82
         version: 8.10.133