diff --git a/.changeset/fix-vite-dev-miniflare-zone.md b/.changeset/fix-vite-dev-miniflare-zone.md
new file mode 100644
index 0000000000..38efdb29b8
--- /dev/null
+++ b/.changeset/fix-vite-dev-miniflare-zone.md
@@ -0,0 +1,9 @@
+---
+"wrangler": patch
+---
+
+Pass the local dev zone through `unstable_getMiniflareWorkerOptions`
+
+When `@cloudflare/vite-plugin` asks Wrangler for Miniflare worker options, the returned object did not include the inferred `zone`. Miniflare then fell back to `<worker>.example.com` for the `CF-Worker` header, which differs from the `wrangler dev --local` path and can cause some upstreams to reject local subrequests.
+
+This now forwards the same `dev.host` or inferred route host that Wrangler already uses in local dev so Vite-backed local development matches the existing local runtime behavior.
diff --git a/packages/wrangler/src/__tests__/unstable-get-miniflare-worker-options.test.ts b/packages/wrangler/src/__tests__/unstable-get-miniflare-worker-options.test.ts
new file mode 100644
index 0000000000..cde1b1416b
--- /dev/null
+++ b/packages/wrangler/src/__tests__/unstable-get-miniflare-worker-options.test.ts
@@ -0,0 +1,61 @@
+import { describe, it } from "vitest";
+import { unstable_getMiniflareWorkerOptions } from "../api";
+import type { Config } from "@cloudflare/workers-utils";
+
+function makeConfig(
+	overrides: Partial<{
+		dev: { host?: string; enable_containers?: boolean; container_engine?: string };
+		route: string;
+		routes: string[];
+	}> = {}
+): Config {
+	return {
+		name: "test-worker",
+		main: "./src/index.ts",
+		compatibility_date: "2025-06-17",
+		compatibility_flags: [],
+		rules: [],
+		queues: { producers: [], consumers: [] },
+		migrations: [],
+		tail_consumers: undefined,
+		streaming_tail_consumers: undefined,
+		containers: [],
+		assets: undefined,
+		define: {},
+		bindings: [],
+		compliance_region: undefined,
+		dev: {
+			ip: "localhost",
+			port: undefined,
+			local_protocol: "http",
+			upstream_protocol: "http",
+			enable_containers: false,
+			...overrides.dev,
+		},
+		...overrides,
+	} as unknown as Config;
+}
+
+describe("unstable_getMiniflareWorkerOptions", () => {
+	it("forwards dev.host as the Miniflare zone", ({ expect }) => {
+		const { workerOptions } = unstable_getMiniflareWorkerOptions(
+			makeConfig({
+				dev: { host: "example.workers.dev" },
+			})
+		);
+
+		expect(workerOptions.zone).toBe("example.workers.dev");
+	});
+
+	it("infers the Miniflare zone from the first route when dev.host is unset", ({
+		expect,
+	}) => {
+		const { workerOptions } = unstable_getMiniflareWorkerOptions(
+			makeConfig({
+				routes: ["https://subdomain.example.com/*"],
+			})
+		);
+
+		expect(workerOptions.zone).toBe("subdomain.example.com");
+	});
+});
diff --git a/packages/wrangler/src/api/integrations/platform/index.ts b/packages/wrangler/src/api/integrations/platform/index.ts
index 364d882d5d..cb2ad126ec 100644
--- a/packages/wrangler/src/api/integrations/platform/index.ts
+++ b/packages/wrangler/src/api/integrations/platform/index.ts
@@ -9,7 +9,7 @@ import { getAssetsOptions } from "../../../assets";
 import { readConfig } from "../../../config";
 import { partitionDurableObjectBindings } from "../../../deployment-bundle/entry";
 import { DEFAULT_MODULE_RULES } from "../../../deployment-bundle/rules";
-import { getBindings } from "../../../dev";
+import { getBindings, getInferredHost } from "../../../dev";
 import { getDurableObjectClassNameToUseSQLiteMap } from "../../../dev/class-names-sqlite";
 import {
 	buildAssetOptions,
@@ -349,6 +349,17 @@ export interface Unstable_MiniflareWorkerOptions {
 	externalWorkers: WorkerOptions[];
 }
 
+function getMiniflareZone(config: Config): string | undefined {
+	if (config.dev.host) {
+		return config.dev.host;
+	}
+
+	return getInferredHost(
+		(config.route && [config.route]) || config.routes,
+		config.configPath
+	);
+}
+
 export function unstable_getMiniflareWorkerOptions(
 	configPath: string,
 	env?: string,
@@ -461,6 +472,7 @@ export function unstable_getMiniflareWorkerOptions(
 		compatibilityDate: config.compatibility_date,
 		compatibilityFlags: config.compatibility_flags,
 		modulesRules,
+		zone: getMiniflareZone(config),
 		containerEngine: useContainers
 			? (config.dev.container_engine ?? resolveDockerHost(getDockerPath()))
 			: undefined,