diff --git a/src/core/AssetUrls.ts b/src/core/AssetUrls.ts
index ae43a8caf..951cf325e 100644
--- a/src/core/AssetUrls.ts
+++ b/src/core/AssetUrls.ts
@@ -30,7 +30,21 @@ export function buildAssetUrl(
   assetManifest: AssetManifest = {},
 ): string {
   const normalizedPath = normalizeAssetPath(path);
-  return assetManifest[normalizedPath] ?? `/${encodeAssetPath(normalizedPath)}`;
+
+  const directUrl = assetManifest[normalizedPath];
+  if (directUrl) {
+    return directUrl;
+  }
+
+  const directoryPrefix = `${normalizedPath}/`;
+  const hasNestedAssets = Object.keys(assetManifest).some((manifestPath) =>
+    manifestPath.startsWith(directoryPrefix),
+  );
+  if (hasNestedAssets) {
+    return `/_assets/${encodeAssetPath(normalizedPath)}`;
+  }
+
+  return `/${encodeAssetPath(normalizedPath)}`;
 }
 
 declare global {
diff --git a/tests/AssetUrls.test.ts b/tests/AssetUrls.test.ts
new file mode 100644
index 000000000..70f5bc581
--- /dev/null
+++ b/tests/AssetUrls.test.ts
@@ -0,0 +1,30 @@
+import { describe, expect, test } from "vitest";
+import { buildAssetUrl } from "../src/core/AssetUrls";
+
+describe("AssetUrls", () => {
+  test("returns hashed URLs for direct asset matches", () => {
+    expect(
+      buildAssetUrl("images/Favicon.svg", {
+        "images/Favicon.svg": "/_assets/images/Favicon.hash.svg",
+      }),
+    ).toBe("/_assets/images/Favicon.hash.svg");
+  });
+
+  test("maps directory prefixes into the hashed asset namespace", () => {
+    const manifest = {
+      "maps/britanniaclassic/manifest.json":
+        "/_assets/maps/britanniaclassic/manifest.hash.json",
+      "maps/britanniaclassic/map.bin":
+        "/_assets/maps/britanniaclassic/map.hash.bin",
+    };
+
+    expect(buildAssetUrl("maps", manifest)).toBe("/_assets/maps");
+    expect(buildAssetUrl("maps/britanniaclassic", manifest)).toBe(
+      "/_assets/maps/britanniaclassic",
+    );
+  });
+
+  test("falls back to the unversioned path when manifest has no match", () => {
+    expect(buildAssetUrl("images/unknown.svg", {})).toBe("/images/unknown.svg");
+  });
+});