diff --git a/__tests__/unit/node/plugins/localSearchPlugin.test.ts b/__tests__/unit/node/plugins/localSearchPlugin.test.ts
index 9f6d4d65..ffbf3e46 100644
--- a/__tests__/unit/node/plugins/localSearchPlugin.test.ts
+++ b/__tests__/unit/node/plugins/localSearchPlugin.test.ts
@@ -1,7 +1,9 @@
 import MiniSearch from 'minisearch'
 import { resolveConfig } from 'node/config'
+import { disposeMdItInstance } from 'node/markdown/markdown'
+import { createMarkdownToVueRenderFn } from 'node/markdownToVue'
 import { localSearchPlugin } from 'node/plugins/localSearchPlugin'
-import { mkdir, mkdtemp, rm, writeFile } from 'node:fs/promises'
+import { mkdir, mkdtemp, readFile, rm, writeFile } from 'node:fs/promises'
 import { tmpdir } from 'node:os'
 import path from 'node:path'
 
@@ -12,6 +14,9 @@ describe('node/plugins/localSearchPlugin', () => {
   beforeEach(() => {
     nodeEnv = process.env.NODE_ENV
     process.env.NODE_ENV = 'production'
+    // createMarkdownRenderer is a module-level singleton keyed on nothing —
+    // reset it so each test's config actually reaches the renderer
+    disposeMdItInstance()
   })
 
   afterEach(async () => {
@@ -102,6 +107,83 @@ describe('node/plugins/localSearchPlugin', () => {
     expect(zhIndex.search('rootonlytoken')).toEqual([])
   })
 
+  test('applies per-locale markdown options (#5350)', async () => {
+    root = await mkdtemp(path.join(tmpdir(), 'vitepress-local-search-'))
+    const configDir = path.join(root, '.vitepress')
+    await mkdir(configDir)
+    await mkdir(path.join(root, 'zh'))
+
+    const content = '::: tip\ntipcontent\n:::\n'
+    await writeFile(path.join(root, 'index.md'), `# Home\n\n${content}`)
+    await writeFile(
+      path.join(root, 'zh', 'index.md'),
+      `# Chinese home\n\n${content}`
+    )
+    await writeFile(
+      path.join(configDir, 'config.ts'),
+      [
+        'export default {',
+        '  locales: {',
+        "    root: { label: 'English', lang: 'en' },",
+        '    zh: {',
+        "      label: 'Chinese',",
+        "      lang: 'zh',",
+        "      markdown: { container: { tipLabel: 'zhtiplabel' } }",
+        '    }',
+        '  },',
+        '  themeConfig: {',
+        "    search: { provider: 'local' }",
+        '  }',
+        '}'
+      ].join('\n')
+    )
+
+    const siteConfig = await resolveConfig(root, 'build', 'production')
+    const plugin = await localSearchPlugin(siteConfig)
+
+    // configResolved hooks run concurrently, so the search plugin may be the
+    // one that creates the shared markdown renderer — page renders must still
+    // pick up per-locale options from it
+    await (plugin.configResolved as any)?.call(
+      {},
+      { publicDir: siteConfig.publicDir }
+    )
+
+    const render = await createMarkdownToVueRenderFn(
+      siteConfig.srcDir,
+      siteConfig.markdown ?? {},
+      siteConfig.site.base,
+      false,
+      false,
+      siteConfig
+    )
+
+    const rootFile = path.join(root, 'index.md')
+    const zhFile = path.join(root, 'zh', 'index.md')
+    const rootPage = await render(await readFile(rootFile, 'utf-8'), rootFile)
+    const zhPage = await render(await readFile(zhFile, 'utf-8'), zhFile)
+    expect(rootPage.vueSrc).toContain('TIP')
+    expect(zhPage.vueSrc).toContain('zhtiplabel')
+
+    // the indexed text must use the localized labels too
+    await (plugin.load as any)?.handler.call({}, '/@localSearchIndex')
+    const rootIndex = loadIndex(
+      (await (plugin.load as any)?.handler.call(
+        {},
+        '/@localSearchIndexroot'
+      )) as string
+    )
+    const zhIndex = loadIndex(
+      (await (plugin.load as any)?.handler.call(
+        {},
+        '/@localSearchIndexzh'
+      )) as string
+    )
+    expect(zhIndex.search('zhtiplabel')).toHaveLength(1)
+    expect(rootIndex.search('zhtiplabel')).toEqual([])
+    expect(rootIndex.search('tip')).toHaveLength(1)
+  })
+
   test('warns and skips pages that fail to render', async () => {
     root = await mkdtemp(path.join(tmpdir(), 'vitepress-local-search-'))
     const configDir = path.join(root, '.vitepress')
diff --git a/src/node/plugins/localSearchPlugin.ts b/src/node/plugins/localSearchPlugin.ts
index 7247d415..35332af3 100644
--- a/src/node/plugins/localSearchPlugin.ts
+++ b/src/node/plugins/localSearchPlugin.ts
@@ -6,7 +6,10 @@ import c from 'picocolors'
 import type { Plugin, ViteDevServer } from 'vite'
 import type { SiteConfig } from '../config'
 import type { DefaultTheme } from '../defaultTheme'
-import { createMarkdownRenderer } from '../markdown/markdown'
+import {
+  createMarkdownRenderer,
+  mergeMarkdownLocales
+} from '../markdown/markdown'
 import { getLocaleForPath, slash, type MarkdownEnv } from '../shared'
 import { readTextFile } from '../utils/fs'
 
@@ -51,10 +54,15 @@ export async function localSearchPlugin(
 
   const options = siteConfig.site.themeConfig.search.options || {}
 
-  async function render(file: string) {
+  async function render(file: string, localeIndex: string) {
     const { srcDir, cleanUrls = false } = siteConfig
     const relativePath = slash(path.relative(srcDir, file))
-    const env: MarkdownEnv = { path: file, relativePath, cleanUrls }
+    const env: MarkdownEnv = {
+      path: file,
+      relativePath,
+      cleanUrls,
+      localeIndex
+    }
     const raw = await readTextFile(file).catch((e) => {
       if (e.code === 'ENOENT') {
         debug(`File not found: ${file}`)
@@ -135,7 +143,7 @@ export async function localSearchPlugin(
     // retrieve file and split into "sections"
     let html: string
     try {
-      html = await render(file)
+      html = await render(file, locale)
     } catch (e) {
       // in dev this runs unawaited, so a page that fails to render must not
       // reject and take the server down with it — the page reports the error
@@ -178,9 +186,12 @@ export async function localSearchPlugin(
     name: 'vitepress:local-search',
 
     async configResolved(config) {
+      // fold in `locales.*.markdown` like markdownToVue does — the renderer
+      // is a singleton, so whichever configResolved hook creates it first
+      // must pass the complete options (#5350)
       md = await createMarkdownRenderer(
         siteConfig.srcDir,
-        siteConfig.markdown,
+        mergeMarkdownLocales(siteConfig.markdown, siteConfig.site.locales),
         siteConfig.site.base,
         siteConfig.logger,
         config.publicDir