diff --git a/CHANGELOG.md b/CHANGELOG.md
index f6099701e7bb..22ffe666981c 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -3110,6 +3110,7 @@ This audited record covers the complete v2026.5.28..v2026.5.31-beta.4 history: 4
 - CLI/context engines: bootstrap and finalize non-legacy context engines for CLI turns while preserving transcript snapshots and deferred maintenance ownership. (#81869) Thanks @sahilsatralkar.
 - Telegram: persist polling updates through restart replay so queued same-topic messages resume in order instead of losing context after a gateway restart. (#82256) Thanks @VACInc.
 - Gateway/Gmail: abort in-flight Gmail watcher startup and hot-reload restarts before shutdown so reloads cannot spawn `gog serve` after the Gateway is closing. Thanks @frankekn.
+- Plugins: reuse compatible current metadata snapshots during runtime load-context resolution, so plugin tool discovery does not discard gateway-provided manifests before auto-enable settles.
 - Agents/Codex: fall back to the embedded PI runner when OpenAI's implicit Codex harness preference cannot find a registered Codex plugin, preventing OpenAI-compatible gateway requests from failing with an unregistered harness error. Fixes #82437.
 - Agents/OpenAI: honor `openai-codex:*` entries placed ahead of API-key backups in `auth.order.openai` for explicit OpenAI PI runs, and accept `models auth login --provider openai-codex --device-code` for headless sign-in. Fixes #82521. (#82605)
 - CLI/channels: install missing externalized same-id channel plugins during `channels add --channel <id>`, so recovery for WhatsApp and other externalized stock channels does not require a separate `plugins enable` step. Fixes #82533.
diff --git a/src/plugins/runtime/load-context.test.ts b/src/plugins/runtime/load-context.test.ts
index 604af3553157..1212d2a3c810 100644
--- a/src/plugins/runtime/load-context.test.ts
+++ b/src/plugins/runtime/load-context.test.ts
@@ -21,6 +21,7 @@ const metadataSnapshot = {
   workspaceDir: "/resolved-workspace",
 };
 const loadPluginMetadataSnapshotMock = vi.fn(() => metadataSnapshot);
+const isPluginMetadataSnapshotCompatibleMock = vi.fn(() => true);
 const getCurrentPluginMetadataSnapshotMock = vi.fn(() => undefined);
 const setCurrentPluginMetadataSnapshotMock = vi.fn();
 const clearCurrentPluginMetadataSnapshotMock = vi.fn();
@@ -45,6 +46,7 @@ vi.mock("../../agents/agent-scope.js", () => ({
 }));
 
 vi.mock("../plugin-metadata-snapshot.js", () => ({
+  isPluginMetadataSnapshotCompatible: isPluginMetadataSnapshotCompatibleMock,
   loadPluginMetadataSnapshot: loadPluginMetadataSnapshotMock,
   resolvePluginMetadataSnapshot: loadPluginMetadataSnapshotMock,
 }));
@@ -69,6 +71,8 @@ describe("resolvePluginRuntimeLoadContext", () => {
     applyPluginAutoEnableMock.mockReset();
     getCurrentPluginMetadataSnapshotMock.mockReset();
     getCurrentPluginMetadataSnapshotMock.mockReturnValue(undefined);
+    isPluginMetadataSnapshotCompatibleMock.mockReset();
+    isPluginMetadataSnapshotCompatibleMock.mockReturnValue(true);
     loadPluginMetadataSnapshotMock.mockClear();
     getCurrentPluginMetadataSnapshotMock.mockClear();
     setCurrentPluginMetadataSnapshotMock.mockClear();
diff --git a/src/plugins/runtime/load-context.ts b/src/plugins/runtime/load-context.ts
index 382e25a7e8ef..b42168c5c778 100644
--- a/src/plugins/runtime/load-context.ts
+++ b/src/plugins/runtime/load-context.ts
@@ -14,7 +14,10 @@ import {
 import { extractPluginInstallRecordsFromInstalledPluginIndex } from "../installed-plugin-index-install-records.js";
 import type { PluginLoadOptions } from "../loader.js";
 import type { PluginManifestRegistry } from "../manifest-registry.js";
-import { resolvePluginMetadataSnapshot } from "../plugin-metadata-snapshot.js";
+import {
+  isPluginMetadataSnapshotCompatible,
+  resolvePluginMetadataSnapshot,
+} from "../plugin-metadata-snapshot.js";
 import type { PluginLogger } from "../types.js";
 
 const log = createSubsystemLogger("plugins");
@@ -73,18 +76,16 @@ export function resolvePluginRuntimeLoadContext(
   const rawConfig = options?.config ?? getRuntimeConfig();
   const rawWorkspaceDir =
     options?.workspaceDir ?? resolveAgentWorkspaceDir(rawConfig, resolveDefaultAgentId(rawConfig));
-  const metadataSnapshot = options?.manifestRegistry
-    ? undefined
-    : resolvePluginMetadataSnapshot({
-        config: rawConfig,
-        env,
-        workspaceDir: rawWorkspaceDir,
-        allowWorkspaceScopedCurrent: true,
-      });
-  const manifestRegistry = options?.manifestRegistry ?? metadataSnapshot?.manifestRegistry;
-  const installRecords = metadataSnapshot
-    ? extractPluginInstallRecordsFromInstalledPluginIndex(metadataSnapshot.index)
-    : undefined;
+  const initialMetadataSnapshot =
+    options?.manifestRegistry === undefined
+      ? resolvePluginMetadataSnapshot({
+          config: rawConfig,
+          env,
+          workspaceDir: rawWorkspaceDir,
+          allowWorkspaceScopedCurrent: true,
+        })
+      : undefined;
+  const manifestRegistry = options?.manifestRegistry ?? initialMetadataSnapshot?.manifestRegistry;
   const activationSourceConfig = resolvePluginActivationSourceConfig({
     config: rawConfig,
     activationSourceConfig: options?.activationSourceConfig,
@@ -93,11 +94,33 @@ export function resolvePluginRuntimeLoadContext(
     config: rawConfig,
     env,
     manifestRegistry,
-    discovery: metadataSnapshot?.discovery,
+    discovery: initialMetadataSnapshot?.discovery,
   });
   const config = autoEnabled.config;
   const workspaceDir =
     options?.workspaceDir ?? resolveAgentWorkspaceDir(config, resolveDefaultAgentId(config));
+  const metadataSnapshot =
+    options?.manifestRegistry !== undefined
+      ? undefined
+      : initialMetadataSnapshot &&
+          isPluginMetadataSnapshotCompatible({
+            snapshot: initialMetadataSnapshot,
+            config,
+            env,
+            workspaceDir,
+          })
+        ? initialMetadataSnapshot
+        : resolvePluginMetadataSnapshot({
+            config,
+            env,
+            workspaceDir,
+            allowWorkspaceScopedCurrent: true,
+            ...(initialMetadataSnapshot ? { index: initialMetadataSnapshot.index } : {}),
+          });
+  const finalManifestRegistry = options?.manifestRegistry ?? metadataSnapshot?.manifestRegistry;
+  const installRecords = metadataSnapshot
+    ? extractPluginInstallRecordsFromInstalledPluginIndex(metadataSnapshot.index)
+    : undefined;
   if (metadataSnapshot) {
     // Reusable snapshots stay available to later manifest-policy lookups for this runtime load.
     if (isReusableCurrentPluginMetadataSnapshot(metadataSnapshot)) {
@@ -119,7 +142,7 @@ export function resolvePluginRuntimeLoadContext(
     workspaceDir,
     env,
     logger: options?.logger ?? createPluginRuntimeLoaderLogger(),
-    manifestRegistry,
+    ...(finalManifestRegistry ? { manifestRegistry: finalManifestRegistry } : {}),
     installRecords,
   };
 }