diff --git a/src/utils/documents.server.ts b/src/utils/documents.server.ts
index d7828d009..6341fec9d 100644
--- a/src/utils/documents.server.ts
+++ b/src/utils/documents.server.ts
@@ -300,7 +300,11 @@ async function fetchFs(repo: string, filepath: string) {
   return null
 }
 
-async function fetchFsFromDevServer(repo: string, filepath: string) {
+async function fetchFsFromDevServer(
+  repo: string,
+  filepath: string,
+  tree = false,
+) {
   let request: Request
 
   try {
@@ -316,6 +320,7 @@ async function fetchFsFromDevServer(repo: string, filepath: string) {
   const url = new URL(localDocsDevPath, request.url)
   url.searchParams.set('repo', repo)
   url.searchParams.set('path', filepath)
+  if (tree) url.searchParams.set('kind', 'tree')
 
   const response = await fetch(url, {
     headers: {
@@ -1429,6 +1434,14 @@ async function fetchApiContentsFs(
   startingPath: string,
 ): Promise<Array<GitHubFileNode> | null> {
   const [_, repo] = repoPair.split('/')
+  if (isIsolateRuntime()) {
+    const text = await fetchFsFromDevServer(repo, startingPath, true)
+    if (text === null) return null
+    const tree: unknown = JSON.parse(text)
+    if (!isGitHubFileNodeArray(tree))
+      throw new Error('Invalid local docs directory response')
+    return tree
+  }
 
   const base = getLocalRepoBaseDirs(repo).find((candidate) =>
     fs.existsSync(path.join(candidate, removeLeadingSlash(startingPath))),
diff --git a/src/utils/local-docs-tree.server.ts b/src/utils/local-docs-tree.server.ts
new file mode 100644
index 000000000..af413ace5
--- /dev/null
+++ b/src/utils/local-docs-tree.server.ts
@@ -0,0 +1,55 @@
+import fs from 'node:fs/promises'
+import path from 'node:path'
+import type { GitHubFileNode } from './documents.server'
+
+const ignored = new Set([
+  'node_modules',
+  '.git',
+  'dist',
+  'test-results',
+  '.output',
+  '.netlify',
+  '.vercel',
+  '.DS_Store',
+  '.nitro',
+])
+
+export async function readLocalDocsTree(
+  repoDir: string,
+  directory: string,
+  depth = 0,
+): Promise<Array<GitHubFileNode>> {
+  const root = await fs.realpath(repoDir)
+  const resolved = await fs.realpath(path.resolve(repoDir, directory))
+  const relative = path.relative(root, resolved)
+  if (
+    relative === '..' ||
+    relative.startsWith(`..${path.sep}`) ||
+    path.isAbsolute(relative)
+  )
+    throw new Error('Directory is outside the repository')
+  const entries = (await fs.readdir(resolved, { withFileTypes: true }))
+    .filter((entry) => !ignored.has(entry.name) && !entry.isSymbolicLink())
+    .sort(
+      (a, b) =>
+        Number(b.isDirectory()) - Number(a.isDirectory()) ||
+        Number(b.name.startsWith('.')) - Number(a.name.startsWith('.')) ||
+        a.name.localeCompare(b.name),
+    )
+  return Promise.all(
+    entries.map(async (entry) => {
+      const filePath = path.posix.join(directory, entry.name)
+      return {
+        name: entry.name,
+        path: filePath,
+        type: entry.isDirectory() ? 'dir' : 'file',
+        depth,
+        parentPath: directory,
+        _links: { self: filePath },
+        ...(entry.isDirectory() && depth <= 3
+          ? { children: await readLocalDocsTree(repoDir, filePath, depth + 1) }
+          : {}),
+      }
+    }),
+  )
+}
diff --git a/tests/local-docs-tree.test.ts b/tests/local-docs-tree.test.ts
new file mode 100644
index 000000000..aaf14421f
--- /dev/null
+++ b/tests/local-docs-tree.test.ts
@@ -0,0 +1,45 @@
+import assert from 'node:assert/strict'
+import { mkdtemp, mkdir, writeFile, symlink, rm } from 'node:fs/promises'
+import os from 'node:os'
+import path from 'node:path'
+import { test } from 'node:test'
+import { readLocalDocsTree } from '../src/utils/local-docs-tree.server'
+
+test('local tree reads nested docs, omits generated directories and symlinks, and stays inside the repo', async () => {
+  const root = await mkdtemp(path.join(os.tmpdir(), 'docs-tree-'))
+  try {
+    const repo = path.join(root, 'repo')
+    await mkdir(path.join(repo, 'docs', 'guide'), { recursive: true })
+    await mkdir(path.join(repo, 'docs', 'node_modules'))
+    await writeFile(path.join(repo, 'docs', 'guide', 'one.md'), '# One')
+    await writeFile(path.join(root, 'outside.md'), 'outside')
+    await symlink(
+      path.join(root, 'outside.md'),
+      path.join(repo, 'docs', 'linked.md'),
+    )
+    const tree = await readLocalDocsTree(repo, 'docs')
+    assert.deepEqual(
+      tree.map((entry) => entry.path),
+      ['docs/guide'],
+    )
+    assert.equal(tree[0].children?.[0].path, 'docs/guide/one.md')
+    assert.equal(tree[0].children?.[0].depth, 1)
+    const rootTree = await readLocalDocsTree(repo, '')
+    assert.deepEqual(
+      rootTree.map((entry) => entry.path),
+      ['docs'],
+    )
+    await mkdir(path.join(repo, '..docs'))
+    await writeFile(path.join(repo, '..docs', 'valid.md'), '# Valid')
+    assert.equal(
+      (await readLocalDocsTree(repo, '..docs'))[0].path,
+      '..docs/valid.md',
+    )
+    await assert.rejects(
+      readLocalDocsTree(repo, '..'),
+      /outside the repository/,
+    )
+  } finally {
+    await rm(root, { recursive: true, force: true })
+  }
+})
diff --git a/vite.config.ts b/vite.config.ts
index 8ae2ecb23..7222fcc3c 100644
--- a/vite.config.ts
+++ b/vite.config.ts
@@ -1,3 +1,4 @@
+import { readLocalDocsTree } from './src/utils/local-docs-tree.server'
 import { sentryTanstackStart } from '@sentry/tanstackstart-react/vite'
 import { defineConfig } from 'vite'
 import type { PluginOption } from 'vite'
@@ -62,11 +63,13 @@ function localDocsDevFiles(): PluginOption {
 
         const repo = url.searchParams.get('repo')
         const filepath = url.searchParams.get('path')
+        const isTree = url.searchParams.get('kind') === 'tree'
 
         if (
           !repo ||
           !/^[a-zA-Z0-9._-]+$/.test(repo) ||
-          !filepath ||
+          filepath === null ||
+          (!isTree && !filepath) ||
           !isContainedRepoPath(filepath)
         ) {
           response.statusCode = 400
@@ -87,29 +90,39 @@ function localDocsDevFiles(): PluginOption {
           ]),
         )
 
-        const localFilePath = repoDirs
+        const localEntry = repoDirs
           .map((repoDir) => ({
             filepath: path.resolve(repoDir, filepath),
             repoDir,
           }))
           .find(
             (candidate) =>
-              isPathInside(candidate.repoDir, candidate.filepath) &&
+              (isPathInside(candidate.repoDir, candidate.filepath) ||
+                (isTree && candidate.repoDir === candidate.filepath)) &&
               fs.existsSync(candidate.filepath) &&
-              fs.statSync(candidate.filepath).isFile(),
-          )?.filepath
+              (isTree
+                ? fs.statSync(candidate.filepath).isDirectory()
+                : fs.statSync(candidate.filepath).isFile()),
+          )
 
-        if (!localFilePath) {
+        if (!localEntry) {
           response.statusCode = 404
           response.end()
           return
         }
 
         try {
-          const content = await fs.promises.readFile(localFilePath)
+          const content = isTree
+            ? JSON.stringify(
+                await readLocalDocsTree(localEntry.repoDir, filepath),
+              )
+            : await fs.promises.readFile(localEntry.filepath)
           response.statusCode = 200
           response.setHeader('Cache-Control', 'no-store')
-          response.setHeader('Content-Type', 'text/plain; charset=utf-8')
+          response.setHeader(
+            'Content-Type',
+            isTree ? 'application/json' : 'text/plain; charset=utf-8',
+          )
           response.end(content)
         } catch (error) {
           next(error)