diff --git a/packages/core/src/plugin/supervisor.ts b/packages/core/src/plugin/supervisor.ts
index 59c9ebd798d..9343424ac25 100644
--- a/packages/core/src/plugin/supervisor.ts
+++ b/packages/core/src/plugin/supervisor.ts
@@ -233,7 +233,7 @@ const layer = Layer.effect(
     const bus = yield* Bus.Service
     const watcher = yield* Watcher.Service
     const fs = yield* FSUtil.Service
-    const ready = yield* Deferred.make<void>()
+    const ready = { current: yield* Deferred.make<void>() }
     let observed = 0
 
     // Configured local plugin files can live outside config roots, where the
@@ -291,7 +291,13 @@ const layer = Layer.effect(
       bus.subscribe([Event.Updated, SdkPlugins.Updated]),
     ).pipe(
       // Make accepted work visible to flush before coalescing the burst.
-      Stream.mapEffect(() => Effect.sync(() => ++observed)),
+      Stream.mapEffect(() =>
+        Effect.gen(function* () {
+          observed++
+          if (yield* Deferred.isDone(ready.current)) ready.current = yield* Deferred.make<void>()
+          return observed
+        }),
+      ),
     )
     yield* Stream.concat(Stream.succeed(0), updates).pipe(
       // Keep observing updates while activation runs, retaining only the latest generation request.
@@ -300,12 +306,12 @@ const layer = Layer.effect(
       Stream.runForEach((target) =>
         Effect.gen(function* () {
           yield* activate()
-          if (observed === target) yield* Deferred.succeed(ready, undefined)
+          if (observed === target) yield* Deferred.succeed(ready.current, undefined)
         }).pipe(Effect.catchCause((cause) => Effect.logError("failed to reload plugins", { cause }))),
       ),
       Effect.forkScoped({ startImmediately: true }),
     )
-    return Service.of({ flush: Deferred.await(ready) })
+    return Service.of({ flush: Effect.suspend(() => Deferred.await(ready.current)) })
   }),
 )
 
diff --git a/packages/core/test/location-layer.test.ts b/packages/core/test/location-layer.test.ts
index a70810d0622..da9e73c3c76 100644
--- a/packages/core/test/location-layer.test.ts
+++ b/packages/core/test/location-layer.test.ts
@@ -305,11 +305,13 @@ describe("LocationServiceMap", () => {
           )
           yield* Deferred.await(started)
 
-          yield* PluginSupervisor.Service.use((supervisor) => supervisor.flush).pipe(
+          const flushFiber = yield* PluginSupervisor.Service.use((supervisor) => supervisor.flush).pipe(
             Effect.provide(context),
-            Effect.timeout("1 second"),
+            Effect.forkChild({ startImmediately: true }),
           )
+          expect(flushFiber.pollUnsafe()).toBeUndefined()
           yield* Deferred.succeed(release, undefined)
+          yield* Fiber.join(flushFiber)
           yield* Deferred.await(completed)
         }),
       ),