diff --git a/test/development/app-dir/agent-rules-refresh/agent-rules-refresh.test.ts b/test/development/app-dir/agent-rules-refresh/agent-rules-refresh.test.ts
new file mode 100644
index 00000000..1766e950
--- /dev/null
+++ b/test/development/app-dir/agent-rules-refresh/agent-rules-refresh.test.ts
@@ -0,0 +1,337 @@
+import execa from 'execa'
+import fs from 'fs'
+import os from 'os'
+import path from 'path'
+import { ensureAgentRulesForDev } from '../../../../packages/next/src/server/lib/app-info-log'
+
+const START = '<!-- BEGIN:nextjs-agent-rules -->'
+const END = '<!-- END:nextjs-agent-rules -->'
+const LEGACY_START = '<!-- NEXT-AGENTS-MD-START -->'
+const LEGACY_END = '<!-- NEXT-AGENTS-MD-END -->'
+const REPO_ROOT = path.resolve(__dirname, '../../../..')
+const CODEMOD_CLI = path.join(
+  REPO_ROOT,
+  'packages/next-codemod/bin/next-codemod.ts'
+)
+const TSX_CLI = require.resolve('tsx/cli')
+
+function occurrences(content: string, value: string) {
+  return content.split(value).length - 1
+}
+
+describe('next dev refreshes managed agent rules from its running sources', () => {
+  const projects: string[] = []
+  const originalClaudeCode = process.env.CLAUDECODE
+
+  function createProject() {
+    const project = fs.mkdtempSync(path.join(os.tmpdir(), 'dev-agent-rules-'))
+    projects.push(project)
+    return project
+  }
+
+  beforeAll(() => {
+    process.env.CLAUDECODE = '1'
+  })
+
+  afterAll(() => {
+    if (originalClaudeCode === undefined) delete process.env.CLAUDECODE
+    else process.env.CLAUDECODE = originalClaudeCode
+    for (const project of projects) {
+      fs.rmSync(project, { recursive: true, force: true })
+    }
+  })
+
+  it('updates in place, preserves adjacent content and CRLF, and is idempotent', () => {
+    const project = createProject()
+    const file = path.join(project, 'AGENTS.md')
+    fs.writeFileSync(
+      file,
+      `# Team rules\r\n\r\nKeep this paragraph.\r\n\r\n${START}\r\nstale rules\r\n${END}\r\n\r\n# Footer\r\nKeep this too.\r\n`
+    )
+
+    ensureAgentRulesForDev(project)
+    const first = fs.readFileSync(file, 'utf8')
+
+    expect(first).toContain('# Team rules\r\n')
+    expect(first).toContain('Keep this paragraph.\r\n')
+    expect(first).toContain('# Footer\r\nKeep this too.\r\n')
+    expect(first).not.toContain('stale rules')
+    expect(first).toContain('node_modules/next/dist/docs/')
+    expect(occurrences(first, START)).toBe(1)
+    expect(occurrences(first, END)).toBe(1)
+    expect(first.replace(/\r\n/g, '')).not.toContain('\n')
+    expect(fs.existsSync(path.join(project, 'CLAUDE.md'))).toBe(false)
+
+    ensureAgentRulesForDev(project)
+    expect(fs.readFileSync(file, 'utf8')).toBe(first)
+  })
+
+  it('rewrites the file hosting the block instead of another agent file', () => {
+    const project = createProject()
+    fs.writeFileSync(
+      path.join(project, 'AGENTS.md'),
+      '# Agent-independent team notes\n'
+    )
+    fs.writeFileSync(
+      path.join(project, 'CLAUDE.md'),
+      `# Claude notes\n\n${START}\nold installed rules\n${END}\n`
+    )
+
+    ensureAgentRulesForDev(project)
+    const agents = fs.readFileSync(path.join(project, 'AGENTS.md'), 'utf8')
+    const claude = fs.readFileSync(path.join(project, 'CLAUDE.md'), 'utf8')
+
+    expect(agents).toBe('# Agent-independent team notes\n')
+    expect(claude).toContain('# Claude notes')
+    expect(claude).not.toContain('old installed rules')
+    expect(claude).toContain('node_modules/next/dist/docs/')
+    expect(occurrences(claude, START)).toBe(1)
+    expect(occurrences(claude, END)).toBe(1)
+  })
+
+  it('migrates a legacy block while preserving user-authored content', () => {
+    const project = createProject()
+    const file = path.join(project, 'AGENTS.md')
+    fs.writeFileSync(
+      file,
+      `# Before\n\n${LEGACY_START}\nlegacy index\n${LEGACY_END}\n\n# After\n`
+    )
+
+    ensureAgentRulesForDev(project)
+    const content = fs.readFileSync(file, 'utf8')
+    expect(content).toContain('# Before')
+    expect(content).toContain('# After')
+    expect(content).not.toContain('legacy index')
+    expect(content).not.toContain(LEGACY_START)
+    expect(content).not.toContain(LEGACY_END)
+    expect(occurrences(content, START)).toBe(1)
+    expect(occurrences(content, END)).toBe(1)
+  })
+
+  it('converges an unterminated current block within two starts', () => {
+    const project = createProject()
+    const file = path.join(project, 'AGENTS.md')
+    fs.writeFileSync(file, `# Keep me\n\n${START}\nunterminated stale rules\n`)
+
+    ensureAgentRulesForDev(project)
+    ensureAgentRulesForDev(project)
+
+    const content = fs.readFileSync(file, 'utf8')
+    expect(content).toContain('# Keep me')
+    expect(content).not.toContain('unterminated stale rules')
+    expect(content).toContain('node_modules/next/dist/docs/')
+    expect(occurrences(content, START)).toBe(1)
+    expect(occurrences(content, END)).toBe(1)
+
+    ensureAgentRulesForDev(project)
+    expect(fs.readFileSync(file, 'utf8')).toBe(content)
+  })
+})
+
+describe('@next/codemod upgrade refreshes adopted rules from upgraded Next.js', () => {
+  type GeneratorMode = 'canonical' | 'missing' | 'throws'
+  const projects: string[] = []
+
+  function createProject({
+    installed,
+    target,
+    generator,
+    agents,
+  }: {
+    installed: string
+    target: string
+    generator: GeneratorMode
+    agents?: string
+  }) {
+    const project = fs.mkdtempSync(path.join(os.tmpdir(), 'rules-upgrade-'))
+    projects.push(project)
+    const bin = path.join(project, 'fake-bin')
+    const nextDir = path.join(project, 'node_modules', 'next')
+    const reactDir = path.join(project, 'node_modules', 'react')
+    fs.mkdirSync(bin, { recursive: true })
+    fs.mkdirSync(nextDir, { recursive: true })
+    fs.mkdirSync(reactDir, { recursive: true })
+    fs.writeFileSync(
+      path.join(project, 'package.json'),
+      JSON.stringify({
+        name: 'upgrade-fixture',
+        private: true,
+        dependencies: {
+          next: installed,
+          react: '19.2.0',
+          'react-dom': '19.2.0',
+        },
+      })
+    )
+    fs.writeFileSync(
+      path.join(nextDir, 'package.json'),
+      JSON.stringify({ name: 'next', version: installed })
+    )
+    fs.writeFileSync(
+      path.join(reactDir, 'package.json'),
+      JSON.stringify({ name: 'react', version: '19.2.0' })
+    )
+    if (agents !== undefined) {
+      fs.writeFileSync(path.join(project, 'AGENTS.md'), agents)
+    }
+
+    const npmShim = path.join(bin, 'npm')
+    fs.writeFileSync(
+      npmShim,
+      `#!/usr/bin/env node
+const fs = require('fs')
+const path = require('path')
+const args = process.argv.slice(2)
+const target = process.env.FAKE_NEXT_TARGET
+if (args[0] === '--silent' && args[1] === 'view') {
+  const query = args[2]
+  if (query.startsWith('next@')) {
+    if (args.includes('--field')) console.log(JSON.stringify(target))
+    else console.log(JSON.stringify({ version: target, peerDependencies: { react: '19.2.0', 'react-dom': '19.2.0' } }))
+  } else if (query.startsWith('react@') || query.startsWith('@types/react@') || query.startsWith('@types/react-dom@')) {
+    console.log(JSON.stringify('19.2.0'))
+  } else {
+    throw new Error('Unexpected npm view: ' + query)
+  }
+} else if (args[0] === 'install') {
+  const nextDir = path.join(process.cwd(), 'node_modules', 'next')
+  fs.writeFileSync(path.join(nextDir, 'package.json'), JSON.stringify({ name: 'next', version: target }))
+  const generatorDir = path.join(nextDir, 'dist', 'server', 'lib')
+  fs.rmSync(path.join(nextDir, 'dist'), { recursive: true, force: true })
+  if (process.env.FAKE_GENERATOR_MODE !== 'missing') {
+    fs.mkdirSync(generatorDir, { recursive: true })
+    const source = process.env.FAKE_GENERATOR_MODE === 'throws'
+      ? "exports.writeAgentFiles = () => { throw new Error('generator failed') }"
+      : ${JSON.stringify(`
+const fs = require('fs')
+const path = require('path')
+const start = '<!-- BEGIN:nextjs-agent-rules -->'
+const end = '<!-- END:nextjs-agent-rules -->'
+const block = start + '\\ncanonical rules supplied by upgraded Next.js\\n' + end
+function update(dir, name) {
+  const file = path.join(dir, name)
+  if (!fs.existsSync(file)) return 'skipped'
+  const content = fs.readFileSync(file, 'utf8')
+  const from = content.indexOf(start)
+  if (from < 0) return 'skipped'
+  const markerEnd = content.indexOf(end, from)
+  const after = markerEnd < 0 ? content.length : markerEnd + end.length
+  const updated = content.slice(0, from) + block + content.slice(after)
+  if (updated === content) return 'unchanged'
+  fs.writeFileSync(file, updated)
+  return 'updated'
+}
+exports.writeAgentFiles = (dir) => {
+  const changed = [update(dir, 'AGENTS.md'), update(dir, 'CLAUDE.md')].includes('updated')
+  return new Proxy({}, { get: () => changed ? 'updated' : 'unchanged' })
+}
+`)}
+    fs.writeFileSync(path.join(generatorDir, 'generate-agent-files.js'), source)
+  }
+} else {
+  throw new Error('Unexpected npm command: ' + args.join(' '))
+}
+`
+    )
+    fs.chmodSync(npmShim, 0o755)
+
+    return {
+      project,
+      target,
+      env: {
+        PATH: `${bin}${path.delimiter}${process.env.PATH}`,
+        FAKE_NEXT_TARGET: target,
+        FAKE_GENERATOR_MODE: generator,
+      },
+    }
+  }
+
+  async function upgrade(fixture: ReturnType<typeof createProject>) {
+    const result = await execa(
+      process.execPath,
+      [TSX_CLI, CODEMOD_CLI, 'upgrade', fixture.target, '--yes'],
+      {
+        cwd: fixture.project,
+        env: { ...process.env, ...fixture.env },
+        reject: false,
+      }
+    )
+    if (result.exitCode !== 0) {
+      throw new Error(`codemod failed:
+${result.stdout}
+${result.stderr}`)
+    }
+  }
+
+  afterAll(() => {
+    for (const project of projects) {
+      fs.rmSync(project, { recursive: true, force: true })
+    }
+  })
+
+  it('uses the newly installed package as source of truth', async () => {
+    const adopted = createProject({
+      installed: '16.3.0-canary.80',
+      target: '16.3.0-canary.99',
+      generator: 'canonical',
+      agents: `# Local rules\n\n${START}\nstale package rules\n${END}\n\n# Tail\n`,
+    })
+
+    await upgrade(adopted)
+    const refreshed = fs.readFileSync(
+      path.join(adopted.project, 'AGENTS.md'),
+      'utf8'
+    )
+    expect(refreshed).toContain('# Local rules')
+    expect(refreshed).toContain('# Tail')
+    expect(refreshed).toContain('canonical rules supplied by upgraded Next.js')
+    expect(refreshed).not.toContain('stale package rules')
+    expect(occurrences(refreshed, START)).toBe(1)
+    expect(fs.existsSync(path.join(adopted.project, 'CLAUDE.md'))).toBe(false)
+  })
+
+  it('does not create agent files for projects that have not adopted a block', async () => {
+    const unadopted = createProject({
+      installed: '16.3.0-canary.80',
+      target: '16.3.0-canary.99',
+      generator: 'canonical',
+    })
+
+    await upgrade(unadopted)
+    expect(fs.existsSync(path.join(unadopted.project, 'AGENTS.md'))).toBe(false)
+    expect(fs.existsSync(path.join(unadopted.project, 'CLAUDE.md'))).toBe(false)
+  })
+
+  it('no-ops when the upgraded package predates the generator', async () => {
+    const oldPackage = createProject({
+      installed: '16.2.0',
+      target: '16.2.9',
+      generator: 'missing',
+      agents: `# Local rules\n\n${START}\nstale package rules\n${END}\n`,
+    })
+
+    await upgrade(oldPackage)
+    expect(
+      fs.readFileSync(path.join(oldPackage.project, 'AGENTS.md'), 'utf8')
+    ).toContain('stale package rules')
+  })
+
+  it('keeps a successful upgrade successful if refreshing fails', async () => {
+    const brokenGenerator = createProject({
+      installed: '16.3.0-canary.80',
+      target: '16.3.0-canary.99',
+      generator: 'throws',
+      agents: `# Local rules\n\n${START}\nstale package rules\n${END}\n`,
+    })
+
+    await expect(upgrade(brokenGenerator)).resolves.toBeUndefined()
+    expect(
+      JSON.parse(
+        fs.readFileSync(
+          path.join(brokenGenerator.project, 'package.json'),
+          'utf8'
+        )
+      ).dependencies.next
+    ).toBe('16.3.0-canary.99')
+  })
+})