diff --git a/src/server/GamePreviewBuilder.ts b/src/server/GamePreviewBuilder.ts
index 33d4be3fb..afd188c11 100644
--- a/src/server/GamePreviewBuilder.ts
+++ b/src/server/GamePreviewBuilder.ts
@@ -3,10 +3,7 @@ import { buildAssetUrl } from "../core/AssetUrls";
 import { ClanTagSchema, GameInfo, UsernameSchema } from "../core/Schemas";
 import { formatPlayerDisplayName } from "../core/Util";
 import { GameMode } from "../core/game/Game";
-import {
-  buildPublicAssetManifest,
-  getResourcesDir,
-} from "./PublicAssetManifest";
+import { getRuntimeAssetManifest } from "./RuntimeAssetManifest";
 
 export const PlayerInfoSchema = z.object({
   clientID: z.string().optional(),
@@ -136,17 +133,14 @@ export function escapeHtml(value: string): string {
     .replace(/'/g, "'");
 }
 
-export function buildPreview(
+export async function buildPreview(
   gameID: string,
   origin: string,
   workerPath: string,
   lobby: GameInfo | null,
   publicInfo: ExternalGameInfo | null,
-): PreviewMeta {
-  const assetManifest =
-    process.env.GAME_ENV === "prod"
-      ? buildPublicAssetManifest(getResourcesDir())
-      : {};
+): Promise<PreviewMeta> {
+  const assetManifest = await getRuntimeAssetManifest();
   const buildAbsoluteAssetUrl = (path: string) =>
     new URL(buildAssetUrl(path, assetManifest), origin).toString();
   const isFinished = !!publicInfo?.info?.end;
diff --git a/src/server/GamePreviewRoute.ts b/src/server/GamePreviewRoute.ts
index 01837ff19..9cf28f263 100644
--- a/src/server/GamePreviewRoute.ts
+++ b/src/server/GamePreviewRoute.ts
@@ -96,7 +96,7 @@ export function registerGamePreviewRoute(opts: {
       }
 
       const origin = requestOrigin(req, config);
-      const meta = buildPreview(
+      const meta = await buildPreview(
         gameID,
         origin,
         config.workerPath(gameID),
diff --git a/src/server/RenderHtml.ts b/src/server/RenderHtml.ts
index e3a939ce6..2b2b3db17 100644
--- a/src/server/RenderHtml.ts
+++ b/src/server/RenderHtml.ts
@@ -2,17 +2,11 @@ import ejs from "ejs";
 import type { Response } from "express";
 import fs from "fs/promises";
 import { buildAssetUrl } from "../core/AssetUrls";
-import {
-  buildPublicAssetManifest,
-  getResourcesDir,
-} from "./PublicAssetManifest";
+import { getRuntimeAssetManifest } from "./RuntimeAssetManifest";
 
 export async function renderHtmlContent(htmlPath: string): Promise<string> {
   const htmlContent = await fs.readFile(htmlPath, "utf-8");
-  const assetManifest =
-    process.env.GAME_ENV === "prod"
-      ? buildPublicAssetManifest(getResourcesDir())
-      : {};
+  const assetManifest = await getRuntimeAssetManifest();
   return ejs.render(htmlContent, {
     gitCommit: JSON.stringify(process.env.GIT_COMMIT ?? "undefined"),
     instanceId: JSON.stringify(process.env.INSTANCE_ID ?? "undefined"),
diff --git a/src/server/RuntimeAssetManifest.ts b/src/server/RuntimeAssetManifest.ts
new file mode 100644
index 000000000..812247889
--- /dev/null
+++ b/src/server/RuntimeAssetManifest.ts
@@ -0,0 +1,29 @@
+import fs from "fs/promises";
+import path from "path";
+import { fileURLToPath } from "url";
+import type { AssetManifest } from "../core/AssetUrls";
+
+const __filename = fileURLToPath(import.meta.url);
+const __dirname = path.dirname(__filename);
+const staticDir = path.join(__dirname, "../../static");
+const manifestPath = path.join(staticDir, "_assets", "asset-manifest.json");
+
+let manifestPromise: Promise<AssetManifest> | null = null;
+
+async function readRuntimeAssetManifest(): Promise<AssetManifest> {
+  const raw = await fs.readFile(manifestPath, "utf8");
+  return JSON.parse(raw) as AssetManifest;
+}
+
+export async function getRuntimeAssetManifest(): Promise<AssetManifest> {
+  if (process.env.GAME_ENV !== "prod") {
+    return {};
+  }
+
+  manifestPromise ??= readRuntimeAssetManifest();
+  return manifestPromise;
+}
+
+export function clearRuntimeAssetManifestCache(): void {
+  manifestPromise = null;
+}