diff --git a/src/gateway/server-plugins.test.ts b/src/gateway/server-plugins.test.ts
index cb345ee7894..a7de207cef5 100644
--- a/src/gateway/server-plugins.test.ts
+++ b/src/gateway/server-plugins.test.ts
@@ -616,4 +616,31 @@ describe("loadGatewayPlugins", () => {
       | undefined;
     expect(dispatched?.marker).toBe("after-mutation");
   });
+
+  test("resolves fallback context lazily when a resolver is registered", async () => {
+    const serverPlugins = serverPluginsModule;
+    const runtime = await createSubagentRuntime(serverPlugins);
+    let currentContext = createTestContext("before-resolver-update");
+
+    serverPlugins.setFallbackGatewayContextResolver(() => currentContext);
+    await runtime.run({ sessionKey: "s-4", message: "before resolver update" });
+    expect(getLastDispatchedContext()).toBe(currentContext);
+
+    currentContext = createTestContext("after-resolver-update");
+    await runtime.run({ sessionKey: "s-4", message: "after resolver update" });
+    expect(getLastDispatchedContext()).toBe(currentContext);
+  });
+
+  test("prefers resolver output over an older fallback context snapshot", async () => {
+    const serverPlugins = serverPluginsModule;
+    const runtime = await createSubagentRuntime(serverPlugins);
+    const staleContext = createTestContext("stale-snapshot");
+    const freshContext = createTestContext("fresh-resolver");
+
+    serverPlugins.setFallbackGatewayContext(staleContext);
+    serverPlugins.setFallbackGatewayContextResolver(() => freshContext);
+
+    await runtime.run({ sessionKey: "s-5", message: "prefer resolver" });
+    expect(getLastDispatchedContext()).toBe(freshContext);
+  });
 });
diff --git a/src/gateway/server-plugins.ts b/src/gateway/server-plugins.ts
index 6f72e5c67c7..3611d834610 100644
--- a/src/gateway/server-plugins.ts
+++ b/src/gateway/server-plugins.ts
@@ -32,16 +32,28 @@ const FALLBACK_GATEWAY_CONTEXT_STATE_KEY: unique symbol = Symbol.for(
 
 type FallbackGatewayContextState = {
   context: GatewayRequestContext | undefined;
+  resolveContext: (() => GatewayRequestContext | undefined) | undefined;
 };
 
 const fallbackGatewayContextState = resolveGlobalSingleton<FallbackGatewayContextState>(
   FALLBACK_GATEWAY_CONTEXT_STATE_KEY,
-  () => ({ context: undefined }),
+  () => ({ context: undefined, resolveContext: undefined }),
 );
 
 export function setFallbackGatewayContext(ctx: GatewayRequestContext): void {
-  // TODO: This startup snapshot can become stale if runtime config/context changes.
   fallbackGatewayContextState.context = ctx;
+  fallbackGatewayContextState.resolveContext = undefined;
+}
+
+export function setFallbackGatewayContextResolver(
+  resolveContext: () => GatewayRequestContext | undefined,
+): void {
+  fallbackGatewayContextState.resolveContext = resolveContext;
+}
+
+function getFallbackGatewayContext(): GatewayRequestContext | undefined {
+  const resolved = fallbackGatewayContextState.resolveContext?.();
+  return resolved ?? fallbackGatewayContextState.context;
 }
 
 type PluginSubagentOverridePolicy = {
@@ -238,7 +250,7 @@ async function dispatchGatewayMethod<T>(
   },
 ): Promise<T> {
   const scope = getPluginRuntimeGatewayRequestScope();
-  const context = scope?.context ?? fallbackGatewayContextState.context;
+  const context = scope?.context ?? getFallbackGatewayContext();
   const isWebchatConnect = scope?.isWebchatConnect ?? (() => false);
   if (!context) {
     throw new Error(
diff --git a/src/gateway/server.impl.ts b/src/gateway/server.impl.ts
index 20dfe75dc50..b1e249271b7 100644
--- a/src/gateway/server.impl.ts
+++ b/src/gateway/server.impl.ts
@@ -103,7 +103,7 @@ import { createSecretsHandlers } from "./server-methods/secrets.js";
 import { hasConnectedMobileNode } from "./server-mobile-nodes.js";
 import { loadGatewayModelCatalog } from "./server-model-catalog.js";
 import { createNodeSubscriptionManager } from "./server-node-subscriptions.js";
-import { loadGatewayPlugins, setFallbackGatewayContext } from "./server-plugins.js";
+import { loadGatewayPlugins, setFallbackGatewayContextResolver } from "./server-plugins.js";
 import { createGatewayReloadHandlers } from "./server-reload-handlers.js";
 import { resolveGatewayRuntimeConfig } from "./server-runtime-config.js";
 import { createGatewayRuntimeState } from "./server-runtime-state.js";
@@ -1126,10 +1126,10 @@ export async function startGatewayServer(
     broadcastVoiceWakeChanged,
   };
 
-  // Store the gateway context as a fallback for plugin subagent dispatch
-  // in non-WS paths (Telegram polling, WhatsApp, etc.) where no per-request
-  // scope is set via AsyncLocalStorage.
-  setFallbackGatewayContext(gatewayRequestContext);
+  // Register a lazy fallback for plugin subagent dispatch in non-WS paths
+  // (Telegram polling, WhatsApp, etc.) so later runtime swaps can expose the
+  // current gateway context without relying on a startup snapshot.
+  setFallbackGatewayContextResolver(() => gatewayRequestContext);
 
   attachGatewayWsHandlers({
     wss,