diff --git a/integration-tests/js-compute/fixtures/app/src/request-cache-key.js b/integration-tests/js-compute/fixtures/app/src/request-cache-key.js
index f5e580080a..b931ad76ac 100644
--- a/integration-tests/js-compute/fixtures/app/src/request-cache-key.js
+++ b/integration-tests/js-compute/fixtures/app/src/request-cache-key.js
@@ -63,7 +63,6 @@ import { routes } from "./routes.js";
     });
     routes.set("/request/constructor/cacheKey", () => {
         const request = new Request('https://www.fastly.com', {cacheKey: 'meow'})
-        request.setCacheKey('meow')
         let error = assert(request.headers.get('fastly-xqd-cache-key'), '404CDD7BC109C432F8CC2443B45BCFE95980F5107215C645236E577929AC3E52', `request.headers.get('fastly-xqd-cache-key'`)
         if (error) { return error }
         return pass()
diff --git a/runtime/fastly/builtins/fetch/request-response.cpp b/runtime/fastly/builtins/fetch/request-response.cpp
index 5a6018e11b..e76f305f07 100644
--- a/runtime/fastly/builtins/fetch/request-response.cpp
+++ b/runtime/fastly/builtins/fetch/request-response.cpp
@@ -1767,6 +1767,7 @@ JSObject *Request::create(JSContext *cx, JS::HandleObject requestInstance, JS::H
   JS::RootedValue body_val(cx);
   JS::RootedValue backend_val(cx);
   JS::RootedValue cache_override(cx);
+  JS::RootedValue cache_key(cx);
   JS::RootedValue fastly_val(cx);
   JS::RootedValue manualFramingHeaders(cx);
   bool hasmanualFramingHeaders;
@@ -1777,6 +1778,7 @@ JSObject *Request::create(JSContext *cx, JS::HandleObject requestInstance, JS::H
         !JS_GetProperty(cx, init, "body", &body_val) ||
         !JS_GetProperty(cx, init, "backend", &backend_val) ||
         !JS_GetProperty(cx, init, "cacheOverride", &cache_override) ||
+        !JS_GetProperty(cx, init, "cacheKey", &cache_key) ||
         !JS_GetProperty(cx, init, "fastly", &fastly_val) ||
         !JS_HasOwnProperty(cx, init, "manualFramingHeaders", &hasmanualFramingHeaders) ||
         !JS_GetProperty(cx, init, "manualFramingHeaders", &manualFramingHeaders)) {
@@ -2074,6 +2076,14 @@ JSObject *Request::create(JSContext *cx, JS::HandleObject requestInstance, JS::H
         JS::GetReservedSlot(input_request, static_cast<uint32_t>(Slots::CacheOverride)));
   }
 
+  // Apply the Fastly Compute-proprietary `cacheKey` property.
+  // (in the input_request case, the header will be copied across normally)
+  if (!cache_key.isUndefined()) {
+    if (!set_cache_key(cx, request, cache_key)) {
+      return nullptr;
+    }
+  }
+
   if (fastly_val.isObject()) {
     JS::RootedValue decompress_response_val(cx);
     JS::RootedObject fastly(cx, fastly_val.toObjectOrNull());
diff --git a/runtime/js-compute-runtime/builtins/request-response.cpp b/runtime/js-compute-runtime/builtins/request-response.cpp
index f4c4dbe261..387c3973cb 100644
--- a/runtime/js-compute-runtime/builtins/request-response.cpp
+++ b/runtime/js-compute-runtime/builtins/request-response.cpp
@@ -1814,6 +1814,7 @@ JSObject *Request::create(JSContext *cx, JS::HandleObject requestInstance, JS::H
   JS::RootedValue body_val(cx);
   JS::RootedValue backend_val(cx);
   JS::RootedValue cache_override(cx);
+  JS::RootedValue cache_key(cx);
   JS::RootedValue fastly_val(cx);
   JS::RootedValue manualFramingHeaders(cx);
   bool hasmanualFramingHeaders;
@@ -1824,6 +1825,7 @@ JSObject *Request::create(JSContext *cx, JS::HandleObject requestInstance, JS::H
         !JS_GetProperty(cx, init, "body", &body_val) ||
         !JS_GetProperty(cx, init, "backend", &backend_val) ||
         !JS_GetProperty(cx, init, "cacheOverride", &cache_override) ||
+        !JS_GetProperty(cx, init, "cacheKey", &cache_key) ||
         !JS_GetProperty(cx, init, "fastly", &fastly_val) ||
         !JS_HasOwnProperty(cx, init, "manualFramingHeaders", &hasmanualFramingHeaders) ||
         !JS_GetProperty(cx, init, "manualFramingHeaders", &manualFramingHeaders)) {
@@ -2119,6 +2121,13 @@ JSObject *Request::create(JSContext *cx, JS::HandleObject requestInstance, JS::H
         request, static_cast<uint32_t>(Slots::CacheOverride),
         JS::GetReservedSlot(input_request, static_cast<uint32_t>(Slots::CacheOverride)));
   }
+  // Apply the Fastly Compute-proprietary `cacheKey` property.
+  // (in the input_request case, the header will be copied across normally)
+  if (!cache_key.isUndefined()) {
+    if (!set_cache_key(cx, request, cache_key)) {
+      return nullptr;
+    }
+  }
 
   if (fastly_val.isObject()) {
     JS::RootedValue decompress_response_val(cx);