diff --git a/fixtures/dev-registry/tests/dev-registry.test.ts b/fixtures/dev-registry/tests/dev-registry.test.ts
index a48cc16caf..7170068472 100644
--- a/fixtures/dev-registry/tests/dev-registry.test.ts
+++ b/fixtures/dev-registry/tests/dev-registry.test.ts
@@ -1216,7 +1216,9 @@ describe("Dev Registry: error handling", () => {
 		);
 
 		// The old-format entry has no debugPortAddress, so the proxy should
-		// return a 503 (not connected) rather than crashing.
+		// return a 503 with the incompatible version message rather than crashing.
+		// We wait specifically for the incompatible message (not the generic "not
+		// found" message) to ensure the file watcher has picked up the entry.
 		await vi.waitFor(async () => {
 			const searchParams = new URLSearchParams({
 				"test-service": "service-worker",
@@ -1226,7 +1228,7 @@ describe("Dev Registry: error handling", () => {
 
 			expect(response.status).toBe(503);
 			expect(await response.text()).toEqual(
-				`Worker "service-worker" not found. Make sure it is running locally.`
+				`Worker "service-worker" is not compatible with this version of the dev server. Please update all Worker instances to the same version.`
 			);
 		}, waitForTimeout);
 	});
diff --git a/packages/miniflare/src/index.ts b/packages/miniflare/src/index.ts
index 34f7ba24a0..1edb8fe360 100644
--- a/packages/miniflare/src/index.ts
+++ b/packages/miniflare/src/index.ts
@@ -2161,7 +2161,7 @@ export class Miniflare {
 					],
 					bindings: [
 						{
-							name: "DEV_REGISTRY_DEBUG_PORT",
+							name: CoreBindings.DEV_REGISTRY_DEBUG_PORT,
 							// workerdDebugPort bindings don't have any additional configuration
 							workerdDebugPort: kVoid,
 						},
@@ -2540,11 +2540,6 @@ export class Miniflare {
 			this.#runtimeEntryURL !== undefined,
 			"Runtime entry URL must be set before registering workers"
 		);
-		// The loopback address is the workerd entry URL (host:port), used by the
-		// local explorer for cross-instance HTTP aggregation.
-		const loopbackAddress = `${this.#runtimeEntryURL.hostname}:${
-			this.#runtimeEntryURL.port
-		}`;
 
 		const entries: [string, WorkerDefinition][] = [];
 		for (const workerOpts of this.#workerOpts) {
@@ -2569,7 +2564,6 @@ export class Miniflare {
 					debugPortAddress,
 					defaultEntrypointService,
 					userWorkerService: getUserServiceName(workerOpts.core.name),
-					loopbackAddress,
 				},
 			]);
 		}
diff --git a/packages/miniflare/src/plugins/core/explorer.ts b/packages/miniflare/src/plugins/core/explorer.ts
index c5105f9b5c..022e3ca69f 100644
--- a/packages/miniflare/src/plugins/core/explorer.ts
+++ b/packages/miniflare/src/plugins/core/explorer.ts
@@ -1,6 +1,12 @@
 import assert from "node:assert";
 import SCRIPT_DO_WRAPPER from "worker:core/do-wrapper";
 import SCRIPT_LOCAL_EXPLORER from "worker:local-explorer/explorer";
+import {
+	kVoid,
+	type Service,
+	type Worker_Binding,
+	type Worker_Module,
+} from "../../runtime";
 import { CoreBindings } from "../../workers";
 import { normaliseDurableObject } from "../do";
 import {
@@ -14,7 +20,6 @@ import {
 	SERVICE_LOCAL_EXPLORER,
 } from "./constants";
 import type { PluginWorkerOptions } from "..";
-import type { Service, Worker_Binding, Worker_Module } from "../../runtime";
 import type { DurableObjectClassNames, WorkflowOption } from "../shared";
 import type {
 	BindingIdMap,
@@ -81,6 +86,11 @@ export function getExplorerServices(
 			name: CoreBindings.JSON_TELEMETRY_CONFIG,
 			json: JSON.stringify(telemetry),
 		},
+		{
+			name: CoreBindings.DEV_REGISTRY_DEBUG_PORT,
+			// workerdDebugPort bindings don't have any additional configuration
+			workerdDebugPort: kVoid,
+		},
 	];
 
 	if (hasDurableObjects) {
diff --git a/packages/miniflare/src/shared/DEV_REGISTRY.md b/packages/miniflare/src/shared/DEV_REGISTRY.md
index 7fc45fdd55..5d226361b7 100644
--- a/packages/miniflare/src/shared/DEV_REGISTRY.md
+++ b/packages/miniflare/src/shared/DEV_REGISTRY.md
@@ -51,7 +51,6 @@ type WorkerDefinition = {
 	debugPortAddress: string; // e.g. "127.0.0.1:12345"
 	defaultEntrypointService: string; // workerd service name for default entrypoint
 	userWorkerService: string; // workerd service name bypassing asset proxies
-	loopbackAddress: string; // e.g. "127.0.0.1:8787"
 };
 ```
 
diff --git a/packages/miniflare/src/shared/dev-registry-types.ts b/packages/miniflare/src/shared/dev-registry-types.ts
index 7a193ef73c..8e81b37308 100644
--- a/packages/miniflare/src/shared/dev-registry-types.ts
+++ b/packages/miniflare/src/shared/dev-registry-types.ts
@@ -19,9 +19,4 @@ export type WorkerDefinition = {
 	 * workers it bypasses the Assets proxy (whether built-in or userland)
 	 */
 	userWorkerService: string;
-	/**
-	 * HTTP loopback address for this miniflare instance (e.g. "127.0.0.1:8787").
-	 * Used by the local explorer for cross-instance aggregation.
-	 */
-	loopbackAddress: string;
 };
diff --git a/packages/miniflare/src/workers/core/constants.ts b/packages/miniflare/src/workers/core/constants.ts
index 7fd91d5dc2..21dba37550 100644
--- a/packages/miniflare/src/workers/core/constants.ts
+++ b/packages/miniflare/src/workers/core/constants.ts
@@ -74,6 +74,7 @@ export const CoreBindings = {
 	SERVICE_CACHE: "MINIFLARE_CACHE",
 	SERVICE_DEV_REGISTRY_PROXY: "MINIFLARE_DEV_REGISTRY_PROXY",
 	JSON_TELEMETRY_CONFIG: "MINIFLARE_TELEMETRY_CONFIG",
+	DEV_REGISTRY_DEBUG_PORT: "DEV_REGISTRY_DEBUG_PORT",
 } as const;
 
 export const ProxyOps = {
diff --git a/packages/miniflare/src/workers/core/dev-registry-proxy-shared.worker.ts b/packages/miniflare/src/workers/core/dev-registry-proxy-shared.worker.ts
index dcf47db371..ce7dbfd3be 100644
--- a/packages/miniflare/src/workers/core/dev-registry-proxy-shared.worker.ts
+++ b/packages/miniflare/src/workers/core/dev-registry-proxy-shared.worker.ts
@@ -48,7 +48,29 @@ export function setRegistry(data: Record<string, RegistryEntry>): void {
  * Look up a worker's registry entry by service name.
  */
 export function resolveTarget(service: string): RegistryEntry | undefined {
-	return registry.get(service);
+	const entry = registry.get(service);
+	if (!entry || !("debugPortAddress" in entry)) {
+		return undefined;
+	}
+	return entry;
+}
+
+/**
+ * Check whether a registry entry exists for the given service, even if it's
+ * from an incompatible wrangler version.
+ */
+export function hasRegistryEntry(service: string): boolean {
+	return registry.has(service);
+}
+
+/**
+ * Return an appropriate error message for a worker that can't be resolved.
+ */
+export function workerNotFoundMessage(service: string): string {
+	if (hasRegistryEntry(service)) {
+		return `Worker "${service}" is not compatible with this version of the dev server. Please update all Worker instances to the same version.`;
+	}
+	return `Worker "${service}" not found. Make sure it is running locally.`;
 }
 
 /**
@@ -130,9 +152,7 @@ export function createProxyDurableObjectClass({
 						// workerd probes DO properties (fetch, alarm, etc.) via the get
 						// trap, and throwing here would crash those internal checks.
 						return () => {
-							throw new Error(
-								`Worker "${scriptName}" not found. Make sure it is running locally.`
-							);
+							throw new Error(workerNotFoundMessage(scriptName));
 						};
 					}
 					return Reflect.get(fetcher, prop);
@@ -144,10 +164,7 @@ export function createProxyDurableObjectClass({
 			const fetcher = this._resolve();
 			if (!fetcher) {
 				return Promise.resolve(
-					new Response(
-						`Worker "${scriptName}" not found. Make sure it is running locally.`,
-						{ status: 503 }
-					)
+					new Response(workerNotFoundMessage(scriptName), { status: 503 })
 				);
 			}
 			return fetcher.fetch(request);
diff --git a/packages/miniflare/src/workers/core/dev-registry-proxy.worker.ts b/packages/miniflare/src/workers/core/dev-registry-proxy.worker.ts
index 6bacde9144..b27e3cf723 100644
--- a/packages/miniflare/src/workers/core/dev-registry-proxy.worker.ts
+++ b/packages/miniflare/src/workers/core/dev-registry-proxy.worker.ts
@@ -3,6 +3,7 @@ import {
 	resolveTarget,
 	tailEventsReplacer,
 	tailEventsReviver,
+	workerNotFoundMessage,
 } from "./dev-registry-proxy-shared.worker";
 import type { WorkerdDebugPortConnector } from "./dev-registry-proxy-shared.worker";
 
@@ -75,9 +76,7 @@ export class ExternalServiceProxy extends WorkerEntrypoint<Env, Props> {
 				}
 
 				if (!target._fetcher) {
-					throw new Error(
-						`Worker "${ctx.props.service}" not found. Make sure it is running locally.`
-					);
+					throw new Error(workerNotFoundMessage(ctx.props.service));
 				}
 				return Reflect.get(target._fetcher, prop);
 			},
@@ -86,19 +85,16 @@ export class ExternalServiceProxy extends WorkerEntrypoint<Env, Props> {
 
 	fetch(request: Request): Promise<Response> | Response {
 		if (!this._fetcher) {
-			return new Response(
-				`Worker "${this.ctx.props.service}" not found. Make sure it is running locally.`,
-				{ status: 503 }
-			);
+			return new Response(workerNotFoundMessage(this.ctx.props.service), {
+				status: 503,
+			});
 		}
 		return this._fetcher.fetch(request);
 	}
 
 	async scheduled(controller: ScheduledController) {
 		if (!this._entryFetcher) {
-			throw new Error(
-				`Worker "${this.ctx.props.service}" not found. Make sure it is running locally.`
-			);
+			throw new Error(workerNotFoundMessage(this.ctx.props.service));
 		}
 		const params = new URLSearchParams();
 		if (controller.cron) {
diff --git a/packages/miniflare/src/workers/local-explorer/aggregation.ts b/packages/miniflare/src/workers/local-explorer/aggregation.ts
index f8e4cb617a..3e5ca07106 100644
--- a/packages/miniflare/src/workers/local-explorer/aggregation.ts
+++ b/packages/miniflare/src/workers/local-explorer/aggregation.ts
@@ -5,6 +5,7 @@
  * any one instance can aggregate data from all instances.
  */
 
+import { env } from "cloudflare:workers";
 import { CorePaths } from "../core";
 import type { WorkerRegistry } from "../../shared/dev-registry-types";
 import type { AppContext } from "./common";
@@ -21,18 +22,19 @@ export const NO_AGGREGATE_HEADER = "X-Miniflare-Explorer-No-Aggregate";
  * Get the unique base URLs of peer instances from the dev registry,
  * excluding the current instance (identified by worker names).
  */
-function getPeerUrls(
+function getPeerDebugPortAddresses(
 	registry: WorkerRegistry,
 	selfWorkerNames: string[]
 ): string[] {
 	const selfSet = new Set(selfWorkerNames);
-	const urls = Object.entries(registry)
+	const addresses = Object.entries(registry)
 		.filter(([name]) => !selfSet.has(name))
-		.map(([, def]) => `http://${def.loopbackAddress}`);
+		.map(([, def]) => def.debugPortAddress)
+		.filter((addr): addr is string => typeof addr === "string");
 	// A single Miniflare process with multiple workers registers multiple
 	// entries in the registry, all sharing the same host:port. We deduplicate
 	// to avoid fetching from the same peer multiple times.
-	return [...new Set(urls)];
+	return [...new Set(addresses)];
 }
 
 export async function getPeerUrlsIfAggregating(
@@ -45,25 +47,29 @@ export async function getPeerUrlsIfAggregating(
 	const workerNames = c.env.LOCAL_EXPLORER_WORKER_NAMES;
 	const response = await loopback.fetch("http://localhost/core/dev-registry");
 	const registry = (await response.json()) as WorkerRegistry;
-	return getPeerUrls(registry, workerNames);
+	return getPeerDebugPortAddresses(registry, workerNames);
 }
 
 /**
  * Fetch data from a peer instance's explorer API.
  * Returns null on any error (silent omission policy).
  *
- * @param peerUrl - Base URL of the peer instance (e.g., "http://127.0.0.1:8788")
+ * @param peerDebugPortAddress - Debug port address of the peer instance (e.g., "127.0.0.1:12345")
  * @param apiPath - API path relative to the explorer API base (e.g., "/d1/database")
  * @param init - Optional fetch init options
  */
 export async function fetchFromPeer(
-	peerUrl: string,
+	peerDebugPortAddress: string,
 	apiPath: string,
 	init?: RequestInit
 ): Promise<Response | null> {
 	try {
-		const url = new URL(`${EXPLORER_API_PATH}${apiPath}`, peerUrl);
-		const response = await fetch(url.toString(), {
+		const client = (env as AppContext["env"]).DEV_REGISTRY_DEBUG_PORT.connect(
+			peerDebugPortAddress
+		);
+		const fetcher = client.getEntrypoint("core:entry");
+		const url = new URL(`http://localhost${EXPLORER_API_PATH}${apiPath}`);
+		const response = await fetcher.fetch(url.toString(), {
 			...init,
 			headers: {
 				...(init?.headers as Record<string, string> | undefined),
diff --git a/packages/miniflare/src/workers/local-explorer/explorer.worker.ts b/packages/miniflare/src/workers/local-explorer/explorer.worker.ts
index 44e44ff49d..e646154182 100644
--- a/packages/miniflare/src/workers/local-explorer/explorer.worker.ts
+++ b/packages/miniflare/src/workers/local-explorer/explorer.worker.ts
@@ -55,6 +55,7 @@ import type {
 } from "../../plugins/core/types";
 import type { WorkerRegistry } from "../../shared/dev-registry-types";
 import type { CoreBindings } from "../core";
+import type { WorkerdDebugPortConnector } from "../core/dev-registry-proxy-shared.worker";
 import type { LocalExplorerWorker } from "./generated";
 
 export type Env = {
@@ -70,6 +71,7 @@ export type Env = {
 	// Per-worker resource bindings for the /local/workers endpoint
 	[CoreBindings.JSON_EXPLORER_WORKER_OPTS]: ExplorerWorkerOpts;
 	[CoreBindings.JSON_TELEMETRY_CONFIG]: { enabled: boolean; deviceId?: string };
+	[CoreBindings.DEV_REGISTRY_DEBUG_PORT]: WorkerdDebugPortConnector;
 };
 
 export type AppBindings = { Bindings: Env };