diff --git a/CHANGELOG.md b/CHANGELOG.md
index 3801ae9d3972..cda136124fd5 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -17,8 +17,9 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 - Discard matched variants with unknown named values ([#18799](https://github.com/tailwindlabs/tailwindcss/pull/18799))
 - Discard matched variants with non-string values ([#18799](https://github.com/tailwindlabs/tailwindcss/pull/18799))
 - Show suggestions for known `matchVariant` values ([#18798](https://github.com/tailwindlabs/tailwindcss/pull/18798))
-- Migrate `aria` theme keys to `@custom-variant` ([#18815](https://github.com/tailwindlabs/tailwindcss/pull/18815))
-- Migrate `data` theme keys to `@custom-variant` ([#18816](https://github.com/tailwindlabs/tailwindcss/pull/18816))
+- Upgrade: Migrate `aria` theme keys to `@custom-variant` ([#18815](https://github.com/tailwindlabs/tailwindcss/pull/18815))
+- Upgrade: Migrate `data` theme keys to `@custom-variant` ([#18816](https://github.com/tailwindlabs/tailwindcss/pull/18816))
+- Upgrade: Migrate `supports` theme keys to `@custom-variant` ([#18817](https://github.com/tailwindlabs/tailwindcss/pull/18817))
 
 ## [4.1.12] - 2025-08-13
 
diff --git a/integrations/upgrade/js-config.test.ts b/integrations/upgrade/js-config.test.ts
index 808b62013f6b..de10250c29a1 100644
--- a/integrations/upgrade/js-config.test.ts
+++ b/integrations/upgrade/js-config.test.ts
@@ -1122,6 +1122,95 @@ test(
   },
 )
 
+test(
+  'migrate supports theme keys to custom variants',
+  {
+    fs: {
+      'package.json': json`
+        {
+          "dependencies": {
+            "tailwindcss": "^3",
+            "@tailwindcss/upgrade": "workspace:^"
+          }
+        }
+      `,
+      'tailwind.config.ts': ts`
+        export default {
+          content: {
+            relative: true,
+            files: ['./src/**/*.html'],
+          },
+          theme: {
+            extend: {
+              supports: {
+                // Automatically handled by bare values (using CSS variable as the value)
+                foo: 'foo: var(--foo)', // parentheses are optional
+                bar: '(bar: var(--bar))',
+
+                // Not automatically handled by bare values because names differ
+                foo: 'bar: var(--foo)', // parentheses are optional
+                bar: '(qux: var(--bar))',
+
+                // Custom
+                grid: 'display: grid',
+              },
+            },
+          },
+        }
+      `,
+      'src/input.css': css`
+        @tailwind base;
+        @tailwind components;
+        @tailwind utilities;
+      `,
+    },
+  },
+  async ({ exec, fs, expect }) => {
+    await exec('npx @tailwindcss/upgrade')
+
+    expect(await fs.dumpFiles('src/*.css')).toMatchInlineSnapshot(`
+      "
+      --- src/input.css ---
+      @import 'tailwindcss';
+
+      @custom-variant supports-foo {
+        @supports (bar: var(--foo)) {
+          @slot;
+        }
+      }
+      @custom-variant supports-bar {
+        @supports ((qux: var(--bar))) {
+          @slot;
+        }
+      }
+      @custom-variant supports-grid {
+        @supports (display: grid) {
+          @slot;
+        }
+      }
+
+      /*
+        The default border color has changed to \`currentcolor\` in Tailwind CSS v4,
+        so we've added these compatibility styles to make sure everything still
+        looks the same as it did with Tailwind CSS v3.
+
+        If we ever want to remove these styles, we need to add an explicit border
+        color utility to any element that depends on these defaults.
+      */
+      @layer base {
+        *,
+        ::after,
+        ::before,
+        ::backdrop,
+        ::file-selector-button {
+          border-color: var(--color-gray-200, currentcolor);
+        }
+      }
+      "
+    `)
+  },
+)
+
 describe('border compatibility', () => {
   test(
     'migrate border compatibility',
diff --git a/packages/@tailwindcss-upgrade/src/codemods/config/migrate-js-config.ts b/packages/@tailwindcss-upgrade/src/codemods/config/migrate-js-config.ts
index c7fb046f4798..24afe56b85b5 100644
--- a/packages/@tailwindcss-upgrade/src/codemods/config/migrate-js-config.ts
+++ b/packages/@tailwindcss-upgrade/src/codemods/config/migrate-js-config.ts
@@ -24,6 +24,7 @@ import {
   isValidOpacityValue,
   isValidSpacingMultiplier,
 } from '../../../../tailwindcss/src/utils/infer-data-type'
+import * as ValueParser from '../../../../tailwindcss/src/value-parser'
 import { findStaticPlugins, type StaticPluginOptions } from '../../utils/extract-static-plugins'
 import { highlight, info, relative } from '../../utils/renderer'
 
@@ -164,6 +165,35 @@ async function migrateTheme(
       }
       delete resolvedConfig.theme.data
     }
+
+    if ('supports' in resolvedConfig.theme) {
+      for (let [key, value] of Object.entries(resolvedConfig.theme.supports ?? {})) {
+        // Will be handled by bare values if the value of the declaration is a
+        // CSS variable.
+        let parsed = ValueParser.parse(`${value}`)
+
+        // Unwrap the parens, e.g.: `(foo: var(--bar))` → `foo: var(--bar)`
+        if (parsed.length === 1 && parsed[0].kind === 'function' && parsed[0].value === '') {
+          parsed = parsed[0].nodes
+        }
+
+        // Verify structure: `foo: var(--bar)`
+        //                    ^^^ ← must match the `key`
+        if (
+          parsed.length === 3 &&
+          parsed[0].kind === 'word' &&
+          parsed[0].value === key &&
+          parsed[2].kind === 'function' &&
+          parsed[2].value === 'var'
+        ) {
+          continue
+        }
+
+        // Create custom variant
+        variants.set(`supports-${key}`, `{@supports(${value}){@slot;}}`)
+      }
+      delete resolvedConfig.theme.supports
+    }
   }
 
   // Convert theme values to CSS custom properties
@@ -242,7 +272,11 @@ async function migrateTheme(
       if (previousRoot !== root) css += '\n'
       previousRoot = root
 
-      css += `@custom-variant ${name} (${selector});\n`
+      if (selector.startsWith('{')) {
+        css += `@custom-variant ${name} ${selector}\n`
+      } else {
+        css += `@custom-variant ${name} (${selector});\n`
+      }
     }
     css += '}\n'
   }
@@ -407,15 +441,11 @@ const ALLOWED_THEME_KEYS = [
   // Used by @tailwindcss/container-queries
   'containers',
 ]
-const BLOCKED_THEME_KEYS = ['supports']
 function onlyAllowedThemeValues(theme: ThemeConfig): boolean {
   for (let key of Object.keys(theme)) {
     if (!ALLOWED_THEME_KEYS.includes(key)) {
       return false
     }
-    if (BLOCKED_THEME_KEYS.includes(key)) {
-      return false
-    }
   }
 
   if ('screens' in theme && typeof theme.screens === 'object' && theme.screens !== null) {