diff --git a/CHANGELOG.md b/CHANGELOG.md
index 04b99390a9d6..2beb44adf8f7 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -14,6 +14,7 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 - Add support for `blocklist` in config files ([#14556](https://github.com/tailwindlabs/tailwindcss/pull/14556))
 - Add `color-scheme` utilities ([#14567](https://github.com/tailwindlabs/tailwindcss/pull/14567))
 - _Experimental_: Migrate `@import "tailwindcss/tailwind.css"` to `@import "tailwindcss"` ([#14514](https://github.com/tailwindlabs/tailwindcss/pull/14514))
+- _Experimental_: Migrate `@apply` utilities with the template codemods ([#14574](https://github.com/tailwindlabs/tailwindcss/pull/14574))
 - _Experimental_: Add template codemods for migrating variant order ([#14524](https://github.com/tailwindlabs/tailwindcss/pull/14524]))
 - _Experimental_: Add template codemods for migrating `bg-gradient-*` utilities to `bg-linear-*` ([#14537](https://github.com/tailwindlabs/tailwindcss/pull/14537]))
 - _Experimental_: Add template codemods for migrating prefixes ([#14557](https://github.com/tailwindlabs/tailwindcss/pull/14557]))
diff --git a/integrations/upgrade/index.test.ts b/integrations/upgrade/index.test.ts
index 7d17299aa8d1..881f40010a78 100644
--- a/integrations/upgrade/index.test.ts
+++ b/integrations/upgrade/index.test.ts
@@ -69,6 +69,10 @@ test(
         @tailwind base;
         @tailwind components;
         @tailwind utilities;
+
+        .btn {
+          @apply !tw__rounded-md tw__px-2 tw__py-1 tw__bg-blue-500 tw__text-white;
+        }
       `,
     },
   },
@@ -83,7 +87,15 @@ test(
       `,
     )
 
-    await fs.expectFileToContain('src/input.css', css`@import 'tailwindcss' prefix(tw);`)
+    await fs.expectFileToContain('src/input.css', css` @import 'tailwindcss' prefix(tw); `)
+    await fs.expectFileToContain(
+      'src/input.css',
+      css`
+        .btn {
+          @apply tw:rounded-md! tw:px-2 tw:py-1 tw:bg-blue-500 tw:text-white;
+        }
+      `,
+    )
   },
 )
 
diff --git a/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.test.ts b/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.test.ts
index f270472d1e65..df6b35d58ae9 100644
--- a/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.test.ts
+++ b/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.test.ts
@@ -1,3 +1,4 @@
+import { __unstable__loadDesignSystem } from '@tailwindcss/node'
 import dedent from 'dedent'
 import postcss from 'postcss'
 import { expect, it } from 'vitest'
@@ -5,7 +6,7 @@ import { migrateAtApply } from './migrate-at-apply'
 
 const css = dedent
 
-function migrate(input: string) {
+function migrateWithoutConfig(input: string) {
   return postcss()
     .use(migrateAtApply())
     .process(input, { from: expect.getState().testPath })
@@ -14,7 +15,7 @@ function migrate(input: string) {
 
 it('should not migrate `@apply`, when there are no issues', async () => {
   expect(
-    await migrate(css`
+    await migrateWithoutConfig(css`
       .foo {
         @apply flex flex-col items-center;
       }
@@ -28,7 +29,7 @@ it('should not migrate `@apply`, when there are no issues', async () => {
 
 it('should append `!` to each utility, when using `!important`', async () => {
   expect(
-    await migrate(css`
+    await migrateWithoutConfig(css`
       .foo {
         @apply flex flex-col !important;
       }
@@ -43,7 +44,7 @@ it('should append `!` to each utility, when using `!important`', async () => {
 // TODO: Handle SCSS syntax
 it.skip('should append `!` to each utility, when using `#{!important}`', async () => {
   expect(
-    await migrate(css`
+    await migrateWithoutConfig(css`
       .foo {
         @apply flex flex-col #{!important};
       }
@@ -57,7 +58,7 @@ it.skip('should append `!` to each utility, when using `#{!important}`', async (
 
 it('should move the legacy `!` prefix, to the new `!` postfix notation', async () => {
   expect(
-    await migrate(css`
+    await migrateWithoutConfig(css`
       .foo {
         @apply !flex flex-col! hover:!items-start items-center;
       }
@@ -68,3 +69,36 @@ it('should move the legacy `!` prefix, to the new `!` postfix notation', async (
     }"
   `)
 })
+
+it('should apply all candidate migration when migrating with a config', async () => {
+  async function migrateWithConfig(input: string) {
+    return postcss()
+      .use(
+        migrateAtApply({
+          designSystem: await __unstable__loadDesignSystem(
+            css`
+              @import 'tailwindcss' prefix(tw);
+            `,
+            { base: __dirname },
+          ),
+          userConfig: {
+            prefix: 'tw_',
+          },
+        }),
+      )
+      .process(input, { from: expect.getState().testPath })
+      .then((result) => result.css)
+  }
+
+  expect(
+    await migrateWithConfig(css`
+      .foo {
+        @apply !tw_flex [color:--my-color] tw_bg-gradient-to-t;
+      }
+    `),
+  ).toMatchInlineSnapshot(`
+    ".foo {
+      @apply tw:flex! tw:[color:var(--my-color)] tw:bg-linear-to-t;
+    }"
+  `)
+})
diff --git a/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.ts b/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.ts
index ebea30e96d6a..487039f48b1b 100644
--- a/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.ts
+++ b/packages/@tailwindcss-upgrade/src/codemods/migrate-at-apply.ts
@@ -1,7 +1,13 @@
 import type { AtRule, Plugin } from 'postcss'
+import type { Config } from 'tailwindcss'
+import type { DesignSystem } from '../../../tailwindcss/src/design-system'
 import { segment } from '../../../tailwindcss/src/utils/segment'
+import { migrateCandidate } from '../template/migrate'
 
-export function migrateAtApply(): Plugin {
+export function migrateAtApply({
+  designSystem,
+  userConfig,
+}: { designSystem?: DesignSystem; userConfig?: Config } = {}): Plugin {
   function migrate(atRule: AtRule) {
     let utilities = atRule.params.split(/(\s+)/)
     let important =
@@ -30,6 +36,12 @@ export function migrateAtApply(): Plugin {
       return [...variants, utility].join(':')
     })
 
+    // If we have a valid designSystem and config setup, we can run all
+    // candidate migrations on each utility
+    if (designSystem && userConfig) {
+      params = params.map((param) => migrateCandidate(designSystem, userConfig, param))
+    }
+
     atRule.params = params.join('').trim()
   }
 
diff --git a/packages/@tailwindcss-upgrade/src/index.ts b/packages/@tailwindcss-upgrade/src/index.ts
index 1bc83ff1617a..573c13f48cd6 100644
--- a/packages/@tailwindcss-upgrade/src/index.ts
+++ b/packages/@tailwindcss-upgrade/src/index.ts
@@ -112,7 +112,11 @@ async function run() {
     // Migrate each file
     await Promise.allSettled(
       files.map((file) =>
-        migrateStylesheet(file, { newPrefix: parsedConfig?.newPrefix ?? undefined }),
+        migrateStylesheet(file, {
+          newPrefix: parsedConfig?.newPrefix ?? undefined,
+          designSystem: parsedConfig?.designSystem,
+          userConfig: parsedConfig?.userConfig,
+        }),
       ),
     )
 
diff --git a/packages/@tailwindcss-upgrade/src/migrate.ts b/packages/@tailwindcss-upgrade/src/migrate.ts
index e4b0aa36ab5a..680e7c67b04c 100644
--- a/packages/@tailwindcss-upgrade/src/migrate.ts
+++ b/packages/@tailwindcss-upgrade/src/migrate.ts
@@ -1,6 +1,8 @@
 import fs from 'node:fs/promises'
 import path from 'node:path'
 import postcss from 'postcss'
+import type { Config } from 'tailwindcss'
+import type { DesignSystem } from '../../tailwindcss/src/design-system'
 import { formatNodes } from './codemods/format-nodes'
 import { migrateAtApply } from './codemods/migrate-at-apply'
 import { migrateAtLayerUtilities } from './codemods/migrate-at-layer-utilities'
@@ -9,11 +11,13 @@ import { migrateTailwindDirectives } from './codemods/migrate-tailwind-directive
 
 export interface MigrateOptions {
   newPrefix?: string
+  designSystem?: DesignSystem
+  userConfig?: Config
 }
 
 export async function migrateContents(contents: string, options: MigrateOptions, file?: string) {
   return postcss()
-    .use(migrateAtApply())
+    .use(migrateAtApply(options))
     .use(migrateAtLayerUtilities())
     .use(migrateMissingLayers())
     .use(migrateTailwindDirectives(options))
diff --git a/packages/@tailwindcss-upgrade/src/template/migrate.ts b/packages/@tailwindcss-upgrade/src/template/migrate.ts
index b6076d80dc25..5dcbddac8f15 100644
--- a/packages/@tailwindcss-upgrade/src/template/migrate.ts
+++ b/packages/@tailwindcss-upgrade/src/template/migrate.ts
@@ -15,11 +15,29 @@ export type Migration = (
   rawCandidate: string,
 ) => string
 
+export const DEFAULT_MIGRATIONS: Migration[] = [
+  prefix,
+  important,
+  automaticVarInjection,
+  bgGradient,
+  variantOrder,
+]
+
+export function migrateCandidate(
+  designSystem: DesignSystem,
+  userConfig: Config,
+  rawCandidate: string,
+): string {
+  for (let migration of DEFAULT_MIGRATIONS) {
+    rawCandidate = migration(designSystem, userConfig, rawCandidate)
+  }
+  return rawCandidate
+}
+
 export default async function migrateContents(
   designSystem: DesignSystem,
   userConfig: Config,
   contents: string,
-  migrations: Migration[] = [prefix, important, bgGradient, automaticVarInjection, variantOrder],
 ): Promise<string> {
   let candidates = await extractRawCandidates(contents)
 
@@ -28,17 +46,10 @@ export default async function migrateContents(
 
   let output = contents
   for (let { rawCandidate, start, end } of candidates) {
-    let needsMigration = false
-    for (let migration of migrations) {
-      let candidate = migration(designSystem, userConfig, rawCandidate)
-      if (rawCandidate !== candidate) {
-        rawCandidate = candidate
-        needsMigration = true
-      }
-    }
+    let migratedCandidate = migrateCandidate(designSystem, userConfig, rawCandidate)
 
-    if (needsMigration) {
-      output = replaceCandidateInContent(output, rawCandidate, start, end)
+    if (migratedCandidate !== rawCandidate) {
+      output = replaceCandidateInContent(output, migratedCandidate, start, end)
     }
   }