diff --git a/packages/opencode/src/server/routes/instance/httpapi/middleware/instance-context.ts b/packages/opencode/src/server/routes/instance/httpapi/middleware/instance-context.ts
index e39eb7394a50..58ebbc03374e 100644
--- a/packages/opencode/src/server/routes/instance/httpapi/middleware/instance-context.ts
+++ b/packages/opencode/src/server/routes/instance/httpapi/middleware/instance-context.ts
@@ -1,8 +1,10 @@
 import { InstanceRef, WorkspaceRef } from "@/effect/instance-ref"
+import { FSUtil } from "@opencode-ai/core/fs-util"
 import { InstanceStore } from "@/project/instance-store"
 import { Effect, Layer } from "effect"
 import { HttpServerResponse } from "effect/unstable/http"
 import { HttpApiMiddleware } from "effect/unstable/httpapi"
+import { notFound } from "../errors"
 import { WorkspaceRouteContext } from "./workspace-routing"
 
 export class InstanceContextMiddleware extends HttpApiMiddleware.Service<
@@ -23,10 +25,18 @@ function decode(input: string): string {
 function provideInstanceContext<E>(
   effect: Effect.Effect<HttpServerResponse.HttpServerResponse, E>,
   store: InstanceStore.Interface,
+  fs: FSUtil.Interface,
 ): Effect.Effect<HttpServerResponse.HttpServerResponse, E, WorkspaceRouteContext> {
   return Effect.gen(function* () {
     const route = yield* WorkspaceRouteContext
-    const ctx = yield* store.load({ directory: decode(route.directory) })
+    const directory = decode(route.directory)
+    // Validate the requested directory before loading: load may return a cached context or resolve a missing child
+    // through an ancestor repository.
+    if (!(yield* fs.isDir(directory))) {
+      return HttpServerResponse.jsonUnsafe(notFound(`Project directory not found: ${directory}`), { status: 404 })
+    }
+
+    const ctx = yield* store.load({ directory })
     return yield* effect.pipe(
       Effect.provideService(InstanceRef, ctx),
       Effect.provideService(WorkspaceRef, route.workspaceID),
@@ -38,6 +48,7 @@ export const instanceContextLayer = Layer.effect(
   InstanceContextMiddleware,
   Effect.gen(function* () {
     const store = yield* InstanceStore.Service
-    return InstanceContextMiddleware.of((effect) => provideInstanceContext(effect, store))
+    const fs = yield* FSUtil.Service
+    return InstanceContextMiddleware.of((effect) => provideInstanceContext(effect, store, fs))
   }),
 )
diff --git a/packages/opencode/test/server/httpapi-instance.test.ts b/packages/opencode/test/server/httpapi-instance.test.ts
index 5bbd6d7cc0d8..ed3d38c2bfd1 100644
--- a/packages/opencode/test/server/httpapi-instance.test.ts
+++ b/packages/opencode/test/server/httpapi-instance.test.ts
@@ -262,4 +262,51 @@ describe("instance HttpApi", () => {
       )
     }),
   )
+
+  it.live("rejects instance requests for missing project directories", () =>
+    Effect.gen(function* () {
+      const parent = yield* tmpdirScoped({ git: true })
+      const dir = `${parent}/deleted-project`
+      const response = yield* HttpClientRequest.get(InstancePaths.path).pipe(directoryHeader(dir), HttpClient.execute)
+
+      expect(response.status).toBe(404)
+      expect(yield* response.json).toEqual({
+        name: "NotFoundError",
+        data: { message: `Project directory not found: ${dir}` },
+      })
+
+      const prompt = yield* HttpClientRequest.post(SessionPaths.promptAsync.replace(":sessionID", "ses_missing")).pipe(
+        directoryHeader(dir),
+        HttpClientRequest.bodyJson({ agent: "build", parts: [{ type: "text", text: "hello" }] }),
+        Effect.flatMap(HttpClient.execute),
+      )
+
+      expect(prompt.status).toBe(404)
+      expect(yield* prompt.json).toEqual({
+        name: "NotFoundError",
+        data: { message: `Project directory not found: ${dir}` },
+      })
+    }),
+  )
+
+  it.live("rejects cached instance requests after the project directory is deleted", () =>
+    Effect.gen(function* () {
+      const parent = yield* tmpdirScoped({ git: true })
+      const dir = `${parent}/deleted-project`
+      const fs = yield* FileSystem.FileSystem
+      yield* fs.makeDirectory(dir, { recursive: true })
+
+      const initial = yield* HttpClientRequest.get(InstancePaths.path).pipe(directoryHeader(dir), HttpClient.execute)
+      expect(initial.status).toBe(200)
+
+      yield* fs.remove(dir, { recursive: true })
+
+      const response = yield* HttpClientRequest.get(InstancePaths.path).pipe(directoryHeader(dir), HttpClient.execute)
+      expect(response.status).toBe(404)
+      expect(yield* response.json).toEqual({
+        name: "NotFoundError",
+        data: { message: `Project directory not found: ${dir}` },
+      })
+    }),
+  )
 })