diff --git a/packages/nuxt/src/core/app.ts b/packages/nuxt/src/core/app.ts
index bb6b6e6925..4a3bbca8fb 100644
--- a/packages/nuxt/src/core/app.ts
+++ b/packages/nuxt/src/core/app.ts
@@ -108,7 +108,8 @@ async function resolveApp (nuxt: Nuxt, app: NuxtApp) {
   // Resolve layouts/ from all config layers
   app.layouts = {}
   for (const config of nuxt.options._layers.map(layer => layer.config)) {
-    const layoutFiles = await resolveFiles(config.srcDir, `${config.dir?.layouts || 'layouts'}/*{${nuxt.options.extensions.join(',')}}`)
+    const layoutDir = (config.rootDir === nuxt.options.rootDir ? nuxt.options : config).dir?.layouts || 'layouts'
+    const layoutFiles = await resolveFiles(config.srcDir, `${layoutDir}/*{${nuxt.options.extensions.join(',')}}`)
     for (const file of layoutFiles) {
       const name = getNameFromPath(file)
       app.layouts[name] = app.layouts[name] || { name, file }
@@ -118,7 +119,8 @@ async function resolveApp (nuxt: Nuxt, app: NuxtApp) {
   // Resolve middleware/ from all config layers
   app.middleware = []
   for (const config of nuxt.options._layers.map(layer => layer.config)) {
-    const middlewareFiles = await resolveFiles(config.srcDir, `${config.dir?.middleware || 'middleware'}/*{${nuxt.options.extensions.join(',')}}`)
+    const middlewareDir = (config.rootDir === nuxt.options.rootDir ? nuxt.options : config).dir?.middleware || 'middleware'
+    const middlewareFiles = await resolveFiles(config.srcDir, `${middlewareDir}/*{${nuxt.options.extensions.join(',')}}`)
     app.middleware.push(...middlewareFiles.map((file) => {
       const name = getNameFromPath(file)
       return { name, path: file, global: hasSuffix(file, '.global') }
@@ -128,12 +130,13 @@ async function resolveApp (nuxt: Nuxt, app: NuxtApp) {
   // Resolve plugins, first extended layers and then base
   app.plugins = []
   for (const config of nuxt.options._layers.map(layer => layer.config).reverse()) {
+    const pluginDir = (config.rootDir === nuxt.options.rootDir ? nuxt.options : config).dir?.plugins || 'plugins'
     app.plugins.push(...[
       ...(config.plugins || []),
       ...config.srcDir
         ? await resolveFiles(config.srcDir, [
-          `${config.dir?.plugins || 'plugins'}/*.{ts,js,mjs,cjs,mts,cts}`,
-          `${config.dir?.plugins || 'plugins'}/*/index.*{ts,js,mjs,cjs,mts,cts}` // TODO: remove, only scan top-level plugins #18418
+          `${pluginDir}/*.{ts,js,mjs,cjs,mts,cts}`,
+          `${pluginDir}/*/index.*{ts,js,mjs,cjs,mts,cts}` // TODO: remove, only scan top-level plugins #18418
         ])
         : []
     ].map(plugin => normalizePlugin(plugin as NuxtPlugin)))
diff --git a/packages/nuxt/src/core/nitro.ts b/packages/nuxt/src/core/nitro.ts
index f17a253389..abe8ce002c 100644
--- a/packages/nuxt/src/core/nitro.ts
+++ b/packages/nuxt/src/core/nitro.ts
@@ -121,7 +121,7 @@ export async function initNitro (nuxt: Nuxt & { _nitro?: Nitro }) {
             baseURL: nuxt.options.app.buildAssetsDir
           },
       ...nuxt.options._layers
-        .map(layer => join(layer.config.srcDir, layer.config.dir?.public || 'public'))
+        .map(layer => join(layer.config.srcDir, (layer.config.rootDir === nuxt.options.rootDir ? nuxt.options : layer.config).dir?.public || 'public'))
         .filter(dir => existsSync(dir))
         .map(dir => ({ dir }))
     ],
diff --git a/packages/nuxt/src/core/nuxt.ts b/packages/nuxt/src/core/nuxt.ts
index 03b4f0a398..150217f046 100644
--- a/packages/nuxt/src/core/nuxt.ts
+++ b/packages/nuxt/src/core/nuxt.ts
@@ -190,9 +190,10 @@ async function initNuxt (nuxt: Nuxt) {
 
   // Automatically register user modules
   for (const config of nuxt.options._layers.map(layer => layer.config).reverse()) {
+    const modulesDir = (config.rootDir === nuxt.options.rootDir ? nuxt.options : config).dir?.modules || 'modules'
     const layerModules = await resolveFiles(config.srcDir, [
-      `${config.dir?.modules || 'modules'}/*{${nuxt.options.extensions.join(',')}}`,
-      `${config.dir?.modules || 'modules'}/*/index{${nuxt.options.extensions.join(',')}}`
+      `${modulesDir}/*{${nuxt.options.extensions.join(',')}}`,
+      `${modulesDir}/*/index{${nuxt.options.extensions.join(',')}}`
     ])
     for (const mod of layerModules) {
       watchedPaths.add(mod)
diff --git a/packages/nuxt/src/pages/module.ts b/packages/nuxt/src/pages/module.ts
index b6c0f5f784..c0ef5a0bc0 100644
--- a/packages/nuxt/src/pages/module.ts
+++ b/packages/nuxt/src/pages/module.ts
@@ -28,7 +28,7 @@ export default defineNuxtModule({
     const useExperimentalTypedPages = nuxt.options.experimental.typedPages
 
     const pagesDirs = nuxt.options._layers.map(
-      layer => resolve(layer.config.srcDir, layer.config.dir?.pages || 'pages')
+      layer => resolve(layer.config.srcDir, (layer.config.rootDir === nuxt.options.rootDir ? nuxt.options : layer.config).dir?.pages || 'pages')
     )
 
     // Disable module (and use universal router) if pages dir do not exists or user has disabled it
@@ -54,10 +54,13 @@ export default defineNuxtModule({
     nuxt.options.pages = await isPagesEnabled()
 
     // Restart Nuxt when pages dir is added or removed
-    const restartPaths = nuxt.options._layers.flatMap(layer => [
-      join(layer.config.srcDir || layer.cwd, 'app/router.options.ts'),
-      join(layer.config.srcDir || layer.cwd, layer.config.dir?.pages || 'pages')
-    ])
+    const restartPaths = nuxt.options._layers.flatMap((layer) => {
+      const pagesDir = (layer.config.rootDir === nuxt.options.rootDir ? nuxt.options : layer.config).dir?.pages || 'pages'
+      return [
+        join(layer.config.srcDir || layer.cwd, 'app/router.options.ts'),
+        join(layer.config.srcDir || layer.cwd, pagesDir)
+      ]
+    })
 
     nuxt.hooks.hook('builder:watch', async (event, relativePath) => {
       const path = resolve(nuxt.options.srcDir, relativePath)
@@ -178,11 +181,14 @@ export default defineNuxtModule({
     })
 
     // Regenerate templates when adding or removing pages
-    const updateTemplatePaths = nuxt.options._layers.flatMap(l => [
-      join(l.config.srcDir || l.cwd, l.config.dir?.pages || 'pages') + '/',
-      join(l.config.srcDir || l.cwd, l.config.dir?.layouts || 'layouts') + '/',
-      join(l.config.srcDir || l.cwd, l.config.dir?.middleware || 'middleware') + '/'
-    ])
+    const updateTemplatePaths = nuxt.options._layers.flatMap((l) => {
+      const dir = (l.config.rootDir === nuxt.options.rootDir ? nuxt.options : l.config).dir
+      return [
+        join(l.config.srcDir || l.cwd, dir?.pages || 'pages') + '/',
+        join(l.config.srcDir || l.cwd, dir?.layouts || 'layouts') + '/',
+        join(l.config.srcDir || l.cwd, dir?.middleware || 'middleware') + '/'
+      ]
+    })
 
     nuxt.hook('builder:watch', async (event, relativePath) => {
       if (event === 'change') { return }
diff --git a/packages/nuxt/src/pages/utils.ts b/packages/nuxt/src/pages/utils.ts
index f745c30309..d07233850e 100644
--- a/packages/nuxt/src/pages/utils.ts
+++ b/packages/nuxt/src/pages/utils.ts
@@ -42,7 +42,7 @@ export async function resolvePagesRoutes (): Promise<NuxtPage[]> {
   const nuxt = useNuxt()
 
   const pagesDirs = nuxt.options._layers.map(
-    layer => resolve(layer.config.srcDir, layer.config.dir?.pages || 'pages')
+    layer => resolve(layer.config.srcDir, (layer.config.rootDir === nuxt.options.rootDir ? nuxt.options : layer.config).dir?.pages || 'pages')
   )
 
   const scannedFiles: ScannedFile[] = []