diff --git a/__tests__/spec/update-script.js b/__tests__/spec/update-script.js
index 9a881d28e7..5f750a65e6 100644
--- a/__tests__/spec/update-script.js
+++ b/__tests__/spec/update-script.js
@@ -540,6 +540,13 @@ describe('update.sh', () => {
         ' D app/assets/javascripts/step-by-step-nav.js'
       ]))
     })
+
+    it('updates app template includes', () => {
+      expect(gitStatus).toEqual(expect.arrayContaining([
+        ' M app/views/includes/head.html',
+        ' M app/views/includes/scripts.html'
+      ]))
+    })
   })
 
   it('can be run as a piped script', async () => {
diff --git a/lib/_update/post.js b/lib/_update/post.js
index 521e06803f..6de7f65330 100644
--- a/lib/_update/post.js
+++ b/lib/_update/post.js
@@ -1,5 +1,7 @@
 const { updateJavascripts } = require('./update-javascripts')
 const { updateScss } = require('./update-scss')
+const { updateIncludes } = require('./update-includes')
 
 updateJavascripts()
 updateScss()
+updateIncludes()
diff --git a/lib/_update/update-includes.js b/lib/_update/update-includes.js
new file mode 100644
index 0000000000..7d962581a4
--- /dev/null
+++ b/lib/_update/update-includes.js
@@ -0,0 +1,19 @@
+const { getProjectVersion, patchUserFile } = require('./util')
+
+async function updateIncludes () {
+  const userVersion = await getProjectVersion()
+
+  // If the user already has version 13 or greater of the kit installed then
+  // their application.js file is all their code and we don't don't want to
+  // change it
+  if (userVersion >= '13.0.0') {
+    return
+  }
+
+  await patchUserFile(userVersion, 'app/views/includes/head.html')
+  await patchUserFile(userVersion, 'app/views/includes/scripts.html')
+}
+
+module.exports = {
+  updateIncludes
+}
diff --git a/lib/_update/update-includes.test.js b/lib/_update/update-includes.test.js
new file mode 100644
index 0000000000..387197921b
--- /dev/null
+++ b/lib/_update/update-includes.test.js
@@ -0,0 +1,202 @@
+/* eslint-env jest */
+
+const fs = require('fs')
+const fsp = require('fs').promises
+const path = require('path')
+
+jest.mock('./util/fetch-original')
+jest.mock('./util', () => {
+  const originalModule = jest.requireActual('./util')
+
+  return {
+    ...originalModule,
+    getProjectVersion: jest.fn(async () => '')
+  }
+})
+const { fetchOriginal: mockFetchOriginal } = require('./util/fetch-original')
+const { getProjectVersion: mockGetProjectVersion } = require('./util')
+const { projectDir } = require('../path-utils')
+
+const { updateIncludes } = require('./update-includes')
+
+const originalIncludesHead = `<!--[if lte IE 8]><link href="/public/stylesheets/application-ie8.css" rel="stylesheet" type="text/css" /><![endif]-->
+<!--[if gt IE 8]><!--><link href="/public/stylesheets/application.css" media="all" rel="stylesheet" type="text/css" /><!--<![endif]-->
+
+{% for stylesheetUrl in extensionConfig.stylesheets %}
+  <link href="{{ stylesheetUrl }}" rel="stylesheet" type="text/css" />
+{% endfor %}
+`
+
+const newIncludesHead = fs.readFileSync(
+  path.join(projectDir, 'app', 'views', 'includes', 'head.html'),
+  'utf8'
+)
+
+const originalIncludesScripts = `<!-- Javascript -->
+<script src="/public/javascripts/jquery-1.11.3.js"></script>
+
+{% for scriptUrl in extensionConfig.scripts %}
+  <script src="{{scriptUrl}}"></script>
+{% endfor %}
+
+<script src="/public/javascripts/application.js"></script>
+
+{% if useAutoStoreData %}
+  <script src="/public/javascripts/auto-store-data.js"></script>
+{% endif %}
+`
+
+const newIncludesScripts = fs.readFileSync(
+  path.join(projectDir, 'app', 'views', 'includes', 'scripts.html'),
+  'utf8'
+)
+
+describe('updateIncludes', () => {
+  let mockCopyFile, mockReadFile, mockWriteFile
+
+  beforeEach(() => {
+    mockGetProjectVersion.mockResolvedValue(
+      '12.1.1'
+    )
+
+    mockFetchOriginal.mockRejectedValue(
+      new Error('fetchOriginal called more times than expected')
+    )
+
+    mockCopyFile = jest.spyOn(fsp, 'copyFile').mockImplementation(async () => {})
+    mockReadFile = jest.spyOn(fsp, 'readFile').mockResolvedValue(async () => {})
+    mockWriteFile = jest.spyOn(fsp, 'writeFile').mockImplementation(async () => {})
+  })
+
+  afterEach(() => {
+    jest.restoreAllMocks()
+  })
+
+  it('replaces app/views/includes/{head.html, scripts.html} if the user has not updated them', async () => {
+    // original head.html
+    mockFetchOriginal.mockResolvedValueOnce(
+      originalIncludesHead
+    )
+    // their head.html
+    mockReadFile.mockResolvedValueOnce(
+      originalIncludesHead
+    )
+    // our head.html
+    mockReadFile.mockResolvedValueOnce(
+      newIncludesHead
+    )
+
+    // original scripts.html
+    mockFetchOriginal.mockResolvedValueOnce(
+      originalIncludesScripts
+    )
+    // their scripts.html
+    mockReadFile.mockResolvedValueOnce(
+      originalIncludesScripts
+    )
+    // our scripts.html
+    mockReadFile.mockResolvedValueOnce(
+      newIncludesScripts
+    )
+
+    await updateIncludes()
+
+    expect(mockCopyFile).toHaveBeenCalledWith(
+      path.join(projectDir, 'update', 'app', 'views', 'includes', 'head.html'),
+      path.join(projectDir, 'app', 'views', 'includes', 'head.html')
+    )
+
+    expect(mockCopyFile).toHaveBeenCalledWith(
+      path.join(projectDir, 'update', 'app', 'views', 'includes', 'scripts.html'),
+      path.join(projectDir, 'app', 'views', 'includes', 'scripts.html')
+    )
+  })
+
+  it('rewrites app/views/includes/{head.html, scripts.html} if the user has added lines to the bottom of the file', async () => {
+    // original head.html
+    mockFetchOriginal.mockResolvedValueOnce(
+      originalIncludesHead
+    )
+    // their head.html
+    mockReadFile.mockResolvedValueOnce(
+      originalIncludesHead + '\n<link href="mystyles.css" rel="stylesheet" type="text/css" />\n'
+    )
+    // our head.html
+    mockReadFile.mockResolvedValueOnce(
+      newIncludesHead
+    )
+
+    // original scripts.html
+    mockFetchOriginal.mockResolvedValueOnce(
+      originalIncludesScripts
+    )
+    // their scripts.html
+    mockReadFile.mockResolvedValueOnce(
+      originalIncludesScripts + '\n<script>callMyCode()</script>\n'
+    )
+    // our scripts.html
+    mockReadFile.mockResolvedValueOnce(
+      newIncludesScripts
+    )
+
+    await updateIncludes()
+
+    expect(mockWriteFile).toHaveBeenCalledWith(
+      path.join(projectDir, 'app', 'views', 'includes', 'head.html'),
+      newIncludesHead + '\n<link href="mystyles.css" rel="stylesheet" type="text/css" />\n',
+      'utf8'
+    )
+
+    expect(mockWriteFile).toHaveBeenCalledWith(
+      path.join(projectDir, 'app', 'views', 'includes', 'scripts.html'),
+      newIncludesScripts + '\n<script>callMyCode()</script>\n',
+      'utf8'
+    )
+  })
+
+  it('rewrites app/views/includes/scripts.html even if it cannot rewrite head.html', async () => {
+    // original head.html
+    mockFetchOriginal.mockResolvedValueOnce(
+      originalIncludesHead
+    )
+    // their head.html
+    mockReadFile.mockResolvedValueOnce(
+      '\n<link href="mystyles.css" rel="stylesheet" type="text/css" />\n'
+    )
+    // our head.html
+    mockReadFile.mockResolvedValueOnce(
+      newIncludesHead
+    )
+
+    // original scripts.html
+    mockFetchOriginal.mockResolvedValueOnce(
+      originalIncludesScripts
+    )
+    // their scripts.html
+    mockReadFile.mockResolvedValueOnce(
+      originalIncludesScripts + '\n<script>callMyCode()</script>\n'
+    )
+    // our scripts.html
+    mockReadFile.mockResolvedValueOnce(
+      newIncludesScripts
+    )
+
+    const mockConsoleWarn = jest.spyOn(global.console, 'warn').mockImplementation(() => {})
+
+    await updateIncludes()
+
+    expect(mockWriteFile).not.toHaveBeenCalledWith(
+      path.join(projectDir, 'app', 'views', 'includes', 'head.html'),
+      newIncludesHead + '\n<link href="mystyles.css" rel="stylesheet" type="text/css" />\n',
+      'utf8'
+    )
+
+    expect(mockWriteFile).toHaveBeenCalledWith(
+      path.join(projectDir, 'app', 'views', 'includes', 'scripts.html'),
+      newIncludesScripts + '\n<script>callMyCode()</script>\n',
+      'utf8'
+    )
+
+    expect(mockConsoleWarn).toHaveBeenCalledTimes(1)
+  })
+})