diff --git a/packages/devtools/client/composables/state.ts b/packages/devtools/client/composables/state.ts
index 1cf01ec0d1..ec33f62f27 100644
--- a/packages/devtools/client/composables/state.ts
+++ b/packages/devtools/client/composables/state.ts
@@ -73,7 +73,8 @@ export interface VfsFile {
 }
 
 export function useVirtualFiles() {
-  return useAsyncState('vfs-list', () => $fetch<VfsData>('/_vfs.json', { baseURL: '/', responseType: 'json' }))
+  // Nitro v3 only serves `/_vfs/**`; the Accept header selects JSON on both Nitro v2 and v3
+  return useAsyncState('vfs-list', () => $fetch<VfsData>('/_vfs/', { baseURL: '/', headers: { accept: 'application/json' }, responseType: 'json' }))
 }
 
 export function useMergedRouteList() {
diff --git a/packages/devtools/client/pages/modules/virtual-files.vue b/packages/devtools/client/pages/modules/virtual-files.vue
index b1dfa945d2..b0bb6e1690 100644
--- a/packages/devtools/client/pages/modules/virtual-files.vue
+++ b/packages/devtools/client/pages/modules/virtual-files.vue
@@ -23,7 +23,7 @@ const current = ref<VfsFile>()
 watchEffect(() => {
   if (!fileId.value)
     return
-  const url = `/_vfs.json/${encodeURIComponent(fileId.value)}`
+  const url = `/_vfs/${encodeURIComponent(fileId.value)}`
   fetch(url, {
     headers: {
       accept: 'application/json',