diff --git a/packages/kit/src/ignore.ts b/packages/kit/src/ignore.ts
index 825c3dbb6c..76e181df62 100644
--- a/packages/kit/src/ignore.ts
+++ b/packages/kit/src/ignore.ts
@@ -1,6 +1,6 @@
 import { existsSync, readFileSync } from 'node:fs'
 import ignore from 'ignore'
-import { join, relative } from 'pathe'
+import { join, relative, resolve } from 'pathe'
 import { tryUseNuxt } from './context'
 
 /**
@@ -16,14 +16,7 @@ export function isIgnored (pathname: string): boolean {
 
   if (!nuxt._ignore) {
     nuxt._ignore = ignore(nuxt.options.ignoreOptions)
-    const resolvedIgnore = nuxt.options.ignore.flatMap(s => resolveGroupSyntax(s))
-
-    nuxt._ignore.add(resolvedIgnore)
-
-    const nuxtignoreFile = join(nuxt.options.rootDir, '.nuxtignore')
-    if (existsSync(nuxtignoreFile)) {
-      nuxt._ignore.add(readFileSync(nuxtignoreFile, 'utf-8'))
-    }
+    nuxt._ignore.add(resolveIgnorePatterns())
   }
 
   const cwds = nuxt.options._layers?.map(layer => layer.cwd).sort((a, b) => b.length - a.length)
@@ -35,6 +28,31 @@ export function isIgnored (pathname: string): boolean {
   return !!(relativePath && nuxt._ignore.ignores(relativePath))
 }
 
+export function resolveIgnorePatterns (relativePath?: string): string[] {
+  const nuxt = tryUseNuxt()
+
+  // Happens with CLI reloads
+  if (!nuxt) {
+    return []
+  }
+
+  if (!nuxt._ignorePatterns) {
+    nuxt._ignorePatterns = nuxt.options.ignore.flatMap(s => resolveGroupSyntax(s))
+
+    const nuxtignoreFile = join(nuxt.options.rootDir, '.nuxtignore')
+    if (existsSync(nuxtignoreFile)) {
+      const contents = readFileSync(nuxtignoreFile, 'utf-8')
+      nuxt._ignorePatterns.push(...contents.trim().split(/\r?\n/))
+    }
+  }
+
+  if (relativePath) {
+    return nuxt._ignorePatterns.map(p => p.startsWith('*') || p.startsWith('!*') ? p : relative(relativePath, resolve(nuxt.options.rootDir, p)))
+  }
+
+  return nuxt._ignorePatterns
+}
+
 /**
  * This function turns string containing groups '**\/*.{spec,test}.{js,ts}' into an array of strings.
  * For example will '**\/*.{spec,test}.{js,ts}' be resolved to:
diff --git a/packages/kit/src/index.ts b/packages/kit/src/index.ts
index cdbba6e351..da2fe614ad 100644
--- a/packages/kit/src/index.ts
+++ b/packages/kit/src/index.ts
@@ -14,7 +14,7 @@ export * from './build'
 export * from './compatibility'
 export * from './components'
 export * from './context'
-export { isIgnored } from './ignore'
+export { isIgnored, resolveIgnorePatterns } from './ignore'
 export * from './layout'
 export * from './pages'
 export * from './plugin'
diff --git a/packages/nuxt/src/core/nitro.ts b/packages/nuxt/src/core/nitro.ts
index 80f66b0892..917df7dc35 100644
--- a/packages/nuxt/src/core/nitro.ts
+++ b/packages/nuxt/src/core/nitro.ts
@@ -3,7 +3,7 @@ import { cpus } from 'node:os'
 import { join, relative, resolve } from 'pathe'
 import { build, copyPublicAssets, createDevServer, createNitro, prepare, prerender, scanHandlers, writeTypes } from 'nitropack'
 import type { Nitro, NitroConfig } from 'nitropack'
-import { logger } from '@nuxt/kit'
+import { logger, resolveIgnorePatterns } from '@nuxt/kit'
 import escapeRE from 'escape-string-regexp'
 import { defu } from 'defu'
 import fsExtra from 'fs-extra'
@@ -207,6 +207,7 @@ export async function initNitro (nuxt: Nuxt & { _nitro?: Nitro }) {
 
   // Resolve user-provided paths
   nitroConfig.srcDir = resolve(nuxt.options.rootDir, nuxt.options.srcDir, nitroConfig.srcDir!)
+  nitroConfig.ignore = [...(nitroConfig.ignore || []), ...resolveIgnorePatterns(nitroConfig.srcDir)]
 
   // Add fallback server for `ssr: false`
   if (!nuxt.options.ssr) {
diff --git a/packages/schema/src/types/nuxt.ts b/packages/schema/src/types/nuxt.ts
index 52f68bb60d..224c1190ca 100644
--- a/packages/schema/src/types/nuxt.ts
+++ b/packages/schema/src/types/nuxt.ts
@@ -59,6 +59,7 @@ export interface Nuxt {
   // Private fields.
   _version: string
   _ignore?: Ignore
+  _ignorePatterns?: string[]
 
   /** The resolved Nuxt configuration. */
   options: NuxtOptions
diff --git a/test/basic.test.ts b/test/basic.test.ts
index dcdd42ab5a..ec0b6ab1be 100644
--- a/test/basic.test.ts
+++ b/test/basic.test.ts
@@ -894,6 +894,14 @@ describe('ignore list', () => {
     const html = await $fetch('/ignore/composables')
     expect(html).toContain('was import ignored: true')
   })
+  it('should ignore scanned nitro handlers in .nuxtignore', async () => {
+    const html = await $fetch('/ignore/scanned')
+    expect(html).not.toContain('this should be ignored')
+  })
+  it.skipIf(isDev())('should ignore public assets in .nuxtignore', async () => {
+    const html = await $fetch('/ignore/public-asset')
+    expect(html).not.toContain('this should be ignored')
+  })
 })
 
 describe('server tree shaking', () => {
diff --git a/test/fixtures/basic/.nuxtignore b/test/fixtures/basic/.nuxtignore
index 03aa617801..59e57a9454 100644
--- a/test/fixtures/basic/.nuxtignore
+++ b/test/fixtures/basic/.nuxtignore
@@ -1 +1,3 @@
 composables/ignored.*
+**/ignore/public-asset
+server/routes/ignore/scanned.ts
diff --git a/test/fixtures/basic/public/ignore/public-asset b/test/fixtures/basic/public/ignore/public-asset
new file mode 100644
index 0000000000..9a0adbcc4b
--- /dev/null
+++ b/test/fixtures/basic/public/ignore/public-asset
@@ -0,0 +1 @@
+this should be ignored
diff --git a/test/fixtures/basic/server/routes/ignore/scanned.ts b/test/fixtures/basic/server/routes/ignore/scanned.ts
new file mode 100644
index 0000000000..8b4f8b7d3b
--- /dev/null
+++ b/test/fixtures/basic/server/routes/ignore/scanned.ts
@@ -0,0 +1,3 @@
+export default defineEventHandler(() => {
+  return 'this should be ignored'
+})