diff --git a/.changeset/fix-load-manifest-graceful-fallback.md b/.changeset/fix-load-manifest-graceful-fallback.md
new file mode 100644
index 000000000..5627f1092
--- /dev/null
+++ b/.changeset/fix-load-manifest-graceful-fallback.md
@@ -0,0 +1,27 @@
+---
+"@opennextjs/cloudflare": patch
+---
+
+fix: handle known optional manifests gracefully in loadManifest/evalManifest patches
+
+Next.js loads certain manifests with `handleMissing: true` (returning `{}` when the file doesn't
+exist). The adapter's build-time glob scan doesn't find these files when they're conditionally
+generated, so the patched function threw at runtime, crashing dynamic routes with 500.
+
+Instead of a blanket catch-all, handle only the specific optional manifests from Next.js
+`route-module.ts`:
+
+- `react-loadable-manifest` (Turbopack per-route, not all routes have dynamic imports)
+- `subresource-integrity-manifest` (only when `experimental.sri` configured)
+- `server-reference-manifest` (App Router only)
+- `dynamic-css-manifest` (Pages Router + Webpack only)
+- `fallback-build-manifest` (only for `/_error` page)
+- `prefetch-hints` (new in Next.js 16.2)
+- `_client-reference-manifest.js` (optional for static metadata routes, evalManifest)
+
+Manifest matching strips `.json` before comparison since some Next.js constants omit
+the extension (`SUBRESOURCE_INTEGRITY_MANIFEST`, `DYNAMIC_CSS_MANIFEST`, etc.).
+
+Unknown manifests still throw to surface genuine errors.
+
+Fixes #1141.
diff --git a/packages/cloudflare/src/cli/build/patches/plugins/load-manifest.ts b/packages/cloudflare/src/cli/build/patches/plugins/load-manifest.ts
index 347288d04..e94973e4b 100644
--- a/packages/cloudflare/src/cli/build/patches/plugins/load-manifest.ts
+++ b/packages/cloudflare/src/cli/build/patches/plugins/load-manifest.ts
@@ -66,6 +66,23 @@ function loadManifest($PATH, $$$ARGS) {
     return process.env.NEXT_BUILD_ID;
 	}
   ${returnManifests}
+  // Known optional manifests \u2014 Next.js loads these with handleMissing: true
+  // (see vercel/next.js packages/next/src/server/route-modules/route-module.ts).
+  // Return {} to match Next.js behaviour instead of crashing the worker.
+  // Note: Some manifest constants in Next.js omit the .json extension
+  // (e.g. SUBRESOURCE_INTEGRITY_MANIFEST, DYNAMIC_CSS_MANIFEST), so we
+  // strip .json before matching to handle both forms.
+  {
+    const p = $PATH.replace(/\\.json$/, "");
+    if (p.endsWith("react-loadable-manifest") ||
+        p.endsWith("subresource-integrity-manifest") ||
+        p.endsWith("server-reference-manifest") ||
+        p.endsWith("dynamic-css-manifest") ||
+        p.endsWith("fallback-build-manifest") ||
+        p.endsWith("prefetch-hints")) {
+      return {};
+    }
+  }
   throw new Error(\`Unexpected loadManifest(\${$PATH}) call!\`);
 }`,
 	} satisfies RuleConfig;
@@ -110,6 +127,11 @@ function evalManifest($PATH, $$$ARGS) {
 function evalManifest($PATH, $$$ARGS) {
   $PATH = $PATH.replaceAll(${JSON.stringify(sep)}, ${JSON.stringify(posix.sep)});
   ${returnManifests}
+  // client-reference-manifest is optional for static metadata routes
+  // (see vercel/next.js route-module.ts, loaded with handleMissing: true)
+  if ($PATH.endsWith("_client-reference-manifest.js")) {
+    return { __RSC_MANIFEST: {} };
+  }
   throw new Error(\`Unexpected evalManifest(\${$PATH}) call!\`);
 }`,
 	} satisfies RuleConfig;