diff --git a/specs/basic_usage.spec.ts b/specs/basic_usage.spec.ts
index e2ab9a241..a47cd5e66 100644
--- a/specs/basic_usage.spec.ts
+++ b/specs/basic_usage.spec.ts
@@ -583,6 +583,10 @@ describe('basic usage', async () => {
       expect(jaRes?.['server-key']).toMatch('こんにちは！')
     })
 
+    test('(#4144) server routes do not set up the i18n server context', async () => {
+      expect(await $fetch('/api/i18n-context')).toEqual({ initialized: false })
+    })
+
     test('(#2220) vue-i18n message compiler works in server routes', async () => {
       const res = await $fetch('/api/vue-i18n-compile')
       expect(res).toMatchObject({ message: 'Hello, nitro!' })
diff --git a/specs/fixtures/basic_usage/server/api/i18n-context.ts b/specs/fixtures/basic_usage/server/api/i18n-context.ts
new file mode 100644
index 000000000..6a7d66bc6
--- /dev/null
+++ b/specs/fixtures/basic_usage/server/api/i18n-context.ts
@@ -0,0 +1,3 @@
+export default defineEventHandler(event => {
+  return { initialized: event.context.nuxtI18n != null }
+})
diff --git a/src/runtime/server/context.ts b/src/runtime/server/context.ts
index 461432cc6..1d858ab85 100644
--- a/src/runtime/server/context.ts
+++ b/src/runtime/server/context.ts
@@ -8,13 +8,6 @@ import { createLocaleConfigs, resolveDefaultLocale } from '../shared/locales'
 import { cloneDeep } from '../shared/messages'
 import { getMergedMessages } from './utils/messages'
 
-export function useI18nContext(event: H3Event) {
-  if (event.context.nuxtI18n == null) {
-    throw new Error('Nuxt I18n server context has not been set up yet.')
-  }
-  return event.context.nuxtI18n
-}
-
 export function tryUseI18nContext(event: H3Event) {
   return event.context.nuxtI18n
 }
@@ -35,20 +28,6 @@ export async function initializeI18nContext(event: H3Event) {
   return ctx
 }
 
-/**
- * Fetches the messages for the specified locale.
- * @internal
- */
-export const fetchMessages = async (locale: string) => {
-  const headers = new Headers({ 'x-nuxt-i18n': 'internal' })
-  if (import.meta.dev) {
-    headers.set('Cache-Control', 'no-cache')
-  }
-  return await $fetch<LocaleMessages<DefineLocaleMessage>>(`${__I18N_SERVER_ROUTE__}/${__I18N_LOCALE_HASHES__[locale]}/${locale}/messages.json`, {
-    headers,
-  })
-}
-
 export function createI18nContext(): NonNullable<H3EventContext['nuxtI18n']> {
   return {
     messages: {},
diff --git a/src/runtime/server/plugin.ts b/src/runtime/server/plugin.ts
index 7b43286d6..4e8af1d7e 100644
--- a/src/runtime/server/plugin.ts
+++ b/src/runtime/server/plugin.ts
@@ -1,7 +1,7 @@
 import { stringify } from 'devalue'
 import { defineI18nMiddleware } from '@intlify/h3'
 import { defineNitroPlugin, useRuntimeConfig, useStorage } from 'nitropack/runtime'
-import { initializeI18nContext, tryUseI18nContext, useI18nContext } from './context'
+import { initializeI18nContext, tryUseI18nContext } from './context'
 import { createUserLocaleDetector } from './utils/locale-detector'
 import { pickNested } from './utils/messages-utils'
 import { isSupportedLocale, resolveDefaultLocale } from '../shared/locales'
@@ -98,15 +98,12 @@ export default defineNitroPlugin(async (nitro) => {
     return { path: relocated, code: runtimeI18n.redirectStatusCode ?? 302, locale, origin }
   }
 
-  nitro.hooks.hook('request', async (event: H3Event) => {
-    await initializeI18nContext(event)
-  })
-
   nitro.hooks.hook('render:before', async (context) => {
-    if (!__I18N_SERVER_REDIRECT__) { return }
     const { event } = context
+    // set up on first use, so requests that render no page (assets, server routes) skip it (#4144)
+    const ctx = tryUseI18nContext(event) || await initializeI18nContext(event)
+    if (!__I18N_SERVER_REDIRECT__) { return }
 
-    const ctx = import.meta.prerender && !event.context.nuxtI18n ? await initializeI18nContext(event) : useI18nContext(event)
     const url = getRequestURL(event)
     const detector = useDetectors(event, detection)
     const localeSegment = detector.route(event.path)
diff --git a/src/runtime/server/routes/messages.ts b/src/runtime/server/routes/messages.ts
index ad2b5464a..05cd870ba 100644
--- a/src/runtime/server/routes/messages.ts
+++ b/src/runtime/server/routes/messages.ts
@@ -1,6 +1,6 @@
 import { defineCachedEventHandler, defineCachedFunction } from 'nitropack/runtime'
 import { createError, defineEventHandler, getRouterParam } from 'h3'
-import { initializeI18nContext, tryUseI18nContext, useI18nContext } from '../context'
+import { initializeI18nContext, tryUseI18nContext } from '../context'
 import { warnMissedMessageFunctions } from '../../shared/messages'
 
 import type { H3Event } from 'h3'
@@ -15,7 +15,7 @@ const _messagesHandler = defineEventHandler(async (event: H3Event) => {
     throw createError({ status: 400, message: 'Locale not specified.' })
   }
 
-  const ctx = useI18nContext(event)
+  const ctx = tryUseI18nContext(event) || await initializeI18nContext(event)
   if (ctx.localeConfigs && locale in ctx.localeConfigs === false) {
     throw createError({ status: 404, message: `Locale '${locale}' not found.` })
   }
@@ -36,7 +36,6 @@ const getCacheKey = (event: H3Event) =>
 async function shouldBypassCache(event: H3Event) {
   const locale = getRouterParam(event, 'locale')
   if (locale == null) { return false }
-  // prerendering may require initializing context
   const ctx = tryUseI18nContext(event) || await initializeI18nContext(event)
   return !ctx.localeConfigs?.[locale]?.cacheable
 }
diff --git a/src/runtime/server/utils/locale-detector.ts b/src/runtime/server/utils/locale-detector.ts
index e90338e4b..d50da5534 100644
--- a/src/runtime/server/utils/locale-detector.ts
+++ b/src/runtime/server/utils/locale-detector.ts
@@ -1,4 +1,4 @@
-import { fetchMessages, tryUseI18nContext } from '../context'
+import { initializeI18nContext, tryUseI18nContext } from '../context'
 import { deepCopy } from '@intlify/shared'
 import { localeDetector } from '#internal/i18n-locale-detector.mjs'
 
@@ -11,7 +11,8 @@ export function createUserLocaleDetector(defaultLocale: string, fallbackLocale:
 
     // Merge messages into i18n context which contains unserializable messages from vue-i18n
     // configurations - read in-process, `$fetch` would serialize message functions away (#3880)
-    const messages = await (tryUseI18nContext(event)?.loadMessages(locale) ?? fetchMessages(locale))
+    const ctx = tryUseI18nContext(event) || await initializeI18nContext(event)
+    const messages = await ctx.loadMessages(locale)
     for (const locale of Object.keys(messages)) {
       i18nCtx.messages![locale] ??= {}
       deepCopy(messages[locale], i18nCtx.messages![locale])