diff --git a/package.json b/package.json
index 9fdc2ed7..8c74e54f 100644
--- a/package.json
+++ b/package.json
@@ -18,8 +18,8 @@
     "packages/redirects",
     "packages/runtime",
     "packages/static",
-    "packages/dev",
     "packages/ai",
+    "packages/dev",
     "packages/nuxt-module",
     "packages/vite-plugin",
     "packages/vite-plugin-tanstack-start"
diff --git a/packages/dev/package.json b/packages/dev/package.json
index b9c49c80..ff832d05 100644
--- a/packages/dev/package.json
+++ b/packages/dev/package.json
@@ -56,6 +56,7 @@
     "vitest": "^3.0.0"
   },
   "dependencies": {
+    "@netlify/ai": "^0.3.3",
     "@netlify/blobs": "10.3.3",
     "@netlify/config": "^23.2.0",
     "@netlify/dev-utils": "4.3.1",
diff --git a/packages/dev/src/main.ts b/packages/dev/src/main.ts
index 3325edd8..e5818ee8 100644
--- a/packages/dev/src/main.ts
+++ b/packages/dev/src/main.ts
@@ -3,6 +3,7 @@ import { IncomingMessage } from 'node:http'
 import path from 'node:path'
 import process from 'node:process'
 
+import { parseAIGatewayContext, setupAIGateway } from '@netlify/ai/bootstrap'
 import { resolveConfig } from '@netlify/config'
 import {
   ensureNetlifyIgnore,
@@ -459,6 +460,35 @@ export class NetlifyDev {
 
     this.#cleanupJobs.push(() => runtime.stop())
 
+    // Bootstrap AI Gateway: Fetch AI Gateway tokens and inject them into env
+    if (this.#features.environmentVariables && config?.api && siteID && config?.siteInfo?.url) {
+      await setupAIGateway({
+        api: config.api,
+        env: config.env || {},
+        siteID,
+        siteURL: config.siteInfo.url,
+      })
+
+      // Inject AI_GATEWAY into process.env via runtime
+      if (config.env.AI_GATEWAY) {
+        runtime.env.set('AI_GATEWAY', config.env.AI_GATEWAY.value)
+
+        // Parse and inject AI Gateway env vars
+        const aiGatewayContext = parseAIGatewayContext(config.env.AI_GATEWAY.value)
+        if (aiGatewayContext) {
+          runtime.env.set('NETLIFY_AI_GATEWAY_KEY', aiGatewayContext.token)
+          runtime.env.set('NETLIFY_AI_GATEWAY_URL', aiGatewayContext.url)
+
+          if (aiGatewayContext.envVars) {
+            for (const envVar of aiGatewayContext.envVars) {
+              runtime.env.set(envVar.key, aiGatewayContext.token)
+              runtime.env.set(envVar.url, aiGatewayContext.url)
+            }
+          }
+        }
+      }
+    }
+
     let serverAddress: string | undefined
 
     // If a custom server has been provided, use it. If not, we must stand up
diff --git a/packages/dev/tsup.config.ts b/packages/dev/tsup.config.ts
index e93f4974..c5ce64ec 100644
--- a/packages/dev/tsup.config.ts
+++ b/packages/dev/tsup.config.ts
@@ -13,5 +13,6 @@ export default defineConfig([
     watch: argv.includes('--watch'),
     platform: 'node',
     bundle: true,
+    external: ['@netlify/ai'],
   },
 ])