diff --git a/.changeset/hungry-crews-tap.md b/.changeset/hungry-crews-tap.md
new file mode 100644
index 000000000000..c4376be1653f
--- /dev/null
+++ b/.changeset/hungry-crews-tap.md
@@ -0,0 +1,5 @@
+---
+"miniflare": patch
+---
+
+fix: api proxy preserve multiple Set-Cookie headers
diff --git a/packages/miniflare/src/workers/core/devalue.ts b/packages/miniflare/src/workers/core/devalue.ts
index a27e6f624765..4255e36e54fd 100644
--- a/packages/miniflare/src/workers/core/devalue.ts
+++ b/packages/miniflare/src/workers/core/devalue.ts
@@ -149,7 +149,7 @@ export function createHTTPReducers(
 ): ReducersRevivers {
 	return {
 		Headers(val) {
-			if (val instanceof impl.Headers) return Object.fromEntries(val);
+			if (val instanceof impl.Headers) return [...val.entries()];
 		},
 		Request(val) {
 			if (val instanceof impl.Request) {
@@ -169,7 +169,7 @@ export function createHTTPRevivers<RS>(
 	return {
 		Headers(value) {
 			assert(typeof value === "object" && value !== null);
-			return new impl.Headers(value as Record<string, string>);
+			return new impl.Headers(value as string[][]);
 		},
 		Request(value) {
 			assert(Array.isArray(value));
diff --git a/packages/miniflare/test/workers/core/serialize.spec.ts b/packages/miniflare/test/workers/core/serialize.spec.ts
index 2c8528b0bfe6..b4e1bba0dacc 100644
--- a/packages/miniflare/test/workers/core/serialize.spec.ts
+++ b/packages/miniflare/test/workers/core/serialize.spec.ts
@@ -1,9 +1,12 @@
 import test from "ava";
 import { parse, stringify } from "devalue";
 import {
+	createHTTPReducers,
+	createHTTPRevivers,
 	structuredSerializableReducers,
 	structuredSerializableRevivers,
 } from "miniflare";
+import { NODE_PLATFORM_IMPL } from "../../../src/plugins/core/proxy/types";
 
 test("serialize RegExp object consisting of only ascii chars", (t) => {
 	const input = new RegExp(/HelloWorld/);
@@ -24,3 +27,24 @@ test("serialize RegExp object containing non-ascii chars", (t) => {
 	const deserialized = parse(serialized, structuredSerializableRevivers);
 	t.deepEqual(deserialized, input);
 });
+
+test("serialize Headers object consisting of multiple Set-Cookie headers", (t) => {
+	const impl = NODE_PLATFORM_IMPL;
+
+	const headers = new impl.Headers([
+		["content-type", "application/json"],
+		["authorization", "Bearer token"],
+	]);
+	headers.append("Set-Cookie", "cookie1=value_for_cookie_1; Path=/; HttpOnly;");
+	headers.append("Set-Cookie", "cookie2=value_for_cookie_2; Path=/; HttpOnly;");
+
+	const serialized = stringify(headers, createHTTPReducers(impl));
+	const deserialized = parse(serialized, createHTTPRevivers(impl));
+	t.true(deserialized instanceof impl.Headers);
+	t.is(deserialized.get("content-type"), "application/json");
+	t.is(deserialized.get("authorization"), "Bearer token");
+	t.deepEqual(deserialized.getSetCookie(), [
+		"cookie1=value_for_cookie_1; Path=/; HttpOnly;",
+		"cookie2=value_for_cookie_2; Path=/; HttpOnly;",
+	]);
+});