diff --git a/packages/nuxt/src/core/nitro.ts b/packages/nuxt/src/core/nitro.ts
index 55dcf1a197..56e72b6d1a 100644
--- a/packages/nuxt/src/core/nitro.ts
+++ b/packages/nuxt/src/core/nitro.ts
@@ -6,7 +6,7 @@ import { randomUUID } from 'uncrypto'
 import { joinURL, withTrailingSlash } from 'ufo'
 import { build, copyPublicAssets, createDevServer, createNitro, prepare, prerender, scanHandlers, writeTypes } from 'nitropack'
 import type { Nitro, NitroConfig } from 'nitropack'
-import { logger, resolveIgnorePatterns, resolveNuxtModule } from '@nuxt/kit'
+import { findPath, logger, resolveIgnorePatterns, resolveNuxtModule } from '@nuxt/kit'
 import escapeRE from 'escape-string-regexp'
 import { defu } from 'defu'
 import fsExtra from 'fs-extra'
@@ -98,7 +98,7 @@ export async function initNitro (nuxt: Nuxt & { _nitro?: Nitro }) {
     baseURL: nuxt.options.app.baseURL,
     virtual: {
       '#internal/nuxt.config.mjs': () => nuxt.vfs['#build/nuxt.config'],
-      '#spa-template': () => `export const template = ${JSON.stringify(spaLoadingTemplate(nuxt))}`
+      '#spa-template': async () => `export const template = ${JSON.stringify(await spaLoadingTemplate(nuxt))}`
     },
     routeRules: {
       '/__nuxt_error': { cache: false }
@@ -377,8 +377,9 @@ export async function initNitro (nuxt: Nuxt & { _nitro?: Nitro }) {
   const nitro = await createNitro(nitroConfig)
 
   // Trigger Nitro reload when SPA loading template changes
+  const spaLoadingTemplateFilePath = await spaLoadingTemplatePath(nuxt)
   nuxt.hook('builder:watch', async (_event, path) => {
-    if (normalize(path) === spaLoadingTemplatePath(nuxt)) {
+    if (normalize(path) === spaLoadingTemplateFilePath) {
       await nitro.hooks.callHook('rollup:reload')
     }
   })
@@ -524,16 +525,20 @@ function relativeWithDot (from: string, to: string) {
   return relative(from, to).replace(/^([^.])/, './$1') || '.'
 }
 
-function spaLoadingTemplatePath (nuxt: Nuxt) {
-  return typeof nuxt.options.spaLoadingTemplate === 'string'
-    ? resolve(nuxt.options.srcDir, nuxt.options.spaLoadingTemplate)
-    : resolve(nuxt.options.srcDir, 'app/spa-loading-template.html')
+async function spaLoadingTemplatePath (nuxt: Nuxt) {
+  if (typeof nuxt.options.spaLoadingTemplate === 'string') {
+    return resolve(nuxt.options.srcDir, nuxt.options.spaLoadingTemplate)
+  }
+
+  const possiblePaths = nuxt.options._layers.map(layer => join(layer.config.srcDir, 'app/spa-loading-template.html'))
+
+  return await findPath(possiblePaths) ?? resolve(nuxt.options.srcDir, 'app/spa-loading-template.html')
 }
 
-function spaLoadingTemplate (nuxt: Nuxt) {
+async function spaLoadingTemplate (nuxt: Nuxt) {
   if (nuxt.options.spaLoadingTemplate === false) { return '' }
 
-  const spaLoadingTemplate = spaLoadingTemplatePath(nuxt)
+  const spaLoadingTemplate = await spaLoadingTemplatePath(nuxt)
 
   try {
     if (existsSync(spaLoadingTemplate)) {
diff --git a/packages/schema/src/config/app.ts b/packages/schema/src/config/app.ts
index f7c42ea260..87c9046025 100644
--- a/packages/schema/src/config/app.ts
+++ b/packages/schema/src/config/app.ts
@@ -181,9 +181,10 @@ export default defineUntypedSchema({
   /**
    * Boolean or a path to an HTML file with the contents of which will be inserted into any HTML page
    * rendered with `ssr: false`.
-   * - If it is unset, it will use `~/app/spa-loading-template.html` if it exists.
+   * - If it is unset, it will use `~/app/spa-loading-template.html` file in one of your layers, if it exists.
    * - If it is false, no SPA loading indicator will be loaded.
-   * - If true, Nuxt will look for `~/app/spa-loading-template.html` file or a default Nuxt image will be used.
+   * - If true, Nuxt will look for `~/app/spa-loading-template.html` file in one of your layers, or a
+   *   default Nuxt image will be used.
    *
    * Some good sources for spinners are [SpinKit](https://github.com/tobiasahlin/SpinKit) or [SVG Spinners](https://icones.js.org/collection/svg-spinners).
    * @example ~/app/spa-loading-template.html
diff --git a/test/basic.test.ts b/test/basic.test.ts
index c3fa14dfac..1b2172c7e3 100644
--- a/test/basic.test.ts
+++ b/test/basic.test.ts
@@ -64,6 +64,11 @@ describe('route rules', () => {
     await expectNoClientErrors('/route-rules/spa')
   })
 
+  it('should not render loading template in spa mode if it is not enabled', async () => {
+    const html = await $fetch('/route-rules/spa')
+    expect(html).toContain('<div id="__nuxt"></div>')
+  })
+
   it('should allow defining route rules inline', async () => {
     const res = await fetch('/route-rules/inline')
     expect(res.status).toEqual(200)