diff --git a/src/runtime/internal/cache.ts b/src/runtime/internal/cache.ts
index 76aad1ce83..ad6a7e1074 100644
--- a/src/runtime/internal/cache.ts
+++ b/src/runtime/internal/cache.ts
@@ -13,6 +13,16 @@ import type { CacheOptions, CachedEventHandlerOptions } from "nitro/types";
 
 let _storageReady = false;
 
+/**
+ * Sanitize a cache group or name so it is safe for filesystem-based storage
+ * drivers (fs, fs-lite). Unstorage maps ":" to "/" on disk, so any "/" already
+ * present in the value would create unexpected directory nesting and cause
+ * ENOTDIR errors when a path is both a file and a prefix of another path.
+ */
+function sanitizeCacheKey(value: string | undefined): string | undefined {
+  return value?.replace(/\//g, "_");
+}
+
 function ensureStorage() {
   if (_storageReady) {
     return;
@@ -37,9 +47,10 @@ export function defineCachedFunction<T, ArgsT extends unknown[] = any[]>(
 ): (...args: ArgsT) => Promise<T> {
   ensureStorage();
   return _defineCachedFunction(fn, {
-    group: "nitro/functions",
     onError: defaultOnError,
     ...opts,
+    group: sanitizeCacheKey(opts.group || "nitro-functions"),
+    name: sanitizeCacheKey(opts.name),
   });
 }
 
@@ -49,12 +60,13 @@ export function defineCachedHandler(
 ): EventHandler {
   ensureStorage();
   const ocacheHandler = _defineCachedHandler(handler as any, {
-    group: "nitro/handlers",
     onError: defaultOnError,
     toResponse: (value, event) => toResponse(value, event as H3Event),
     createResponse: (body, init) => new FastResponse(body, init),
     handleCacheHeaders: (event, conditions) => handleCacheHeaders(event as H3Event, conditions),
     ...opts,
+    group: sanitizeCacheKey(opts.group || "nitro-handlers"),
+    name: sanitizeCacheKey(opts.name),
   });
   return defineHandler((event) => ocacheHandler(event as any));
 }
diff --git a/src/runtime/internal/route-rules.ts b/src/runtime/internal/route-rules.ts
index 1100bc50a6..482e76b657 100644
--- a/src/runtime/internal/route-rules.ts
+++ b/src/runtime/internal/route-rules.ts
@@ -70,9 +70,14 @@ export const cache: RouteRuleCtor<"cache"> = ((m) =>
     const key = `${m.route}:${route}`;
     let cachedHandler = cachedHandlers.get(key);
     if (!cachedHandler) {
+      // Sanitize the name to avoid filesystem path conflicts.
+      // Route paths contain "/" which unstorage's fs drivers interpret as
+      // directory separators, causing ENOTDIR when a path like "/foo" is
+      // cached as a file but "/foo/bar" needs it to be a directory.
+      const safeName = key.replace(/\//g, "_");
       cachedHandler = defineCachedHandler(handler, {
-        group: "nitro/route-rules",
-        name: key,
+        group: "nitro-route-rules",
+        name: safeName,
         ...m.options,
       });
       cachedHandlers.set(key, cachedHandler);