diff --git a/packages/core/src/effect/app-node-builder.ts b/packages/core/src/effect/app-node-builder.ts
index dfefbf8d6620..0f4f8961e834 100644
--- a/packages/core/src/effect/app-node-builder.ts
+++ b/packages/core/src/effect/app-node-builder.ts
@@ -2,6 +2,7 @@ import { buildLocationServiceMap } from "../location-services.js"
 import { LocationServiceMap } from "../location-service-map.js"
 import { LayerNode } from "@opencode/util/effect/layer-node"
 import { makeGlobalNode } from "@opencode/util/effect/app-node"
+import { FSUtil } from "@opencode/util/fs-util"
 import { Effect, Layer } from "effect"
 import { Instance } from "../instance/service.js"
 
@@ -22,7 +23,16 @@ const instances = makeGlobalNode({
 export function build<A, E>(root: LayerNode.Graph<A, E>, replacements: LayerNode.Replacements = []) {
   const bindings = [Instance.node.replace(instances), ...replacements]
   return LayerNode.compile(root, {
-    replacements: [LocationServiceMap.node.replace(buildLocationServiceMap(bindings)), ...bindings],
+    replacements: [
+      LocationServiceMap.node.replace(
+        makeGlobalNode({
+          service: LocationServiceMap.Service,
+          layer: buildLocationServiceMap(bindings),
+          deps: [FSUtil.node],
+        }),
+      ),
+      ...bindings,
+    ],
   })
 }
 
diff --git a/packages/core/src/location-services.ts b/packages/core/src/location-services.ts
index 095811cc39a7..7df80b63933d 100644
--- a/packages/core/src/location-services.ts
+++ b/packages/core/src/location-services.ts
@@ -4,12 +4,26 @@ import { Instance } from "./instance.js"
 import { Location } from "./location.js"
 import { LocationLifecycle } from "./location-lifecycle.js"
 import { LocationServiceMap } from "./location-service-map.js"
+import { FSUtil } from "@opencode/util/fs-util"
+import type { PlatformError } from "effect/PlatformError"
 
 export { LocationServiceMap } from "./location-service-map.js"
 
 export type LocationServices = Instance.Services
 export type LocationError = Instance.Error
 
+export class DirectoryNotFoundError extends Error {
+  constructor(readonly directory: string) {
+    super(`Project directory not found: ${directory}`)
+  }
+}
+
+export class PermissionDeniedError extends Error {
+  constructor(readonly directory: string) {
+    super(`Cannot access project directory: ${directory}`)
+  }
+}
+
 export function buildLocationServiceMap(
   replacements: LayerNode.Replacements = [],
 ): Layer.Layer<LocationServiceMap.Service> {
@@ -17,6 +31,7 @@ export function buildLocationServiceMap(
     LocationServiceMap.Service,
     Effect.gen(function* () {
       const owner = yield* Effect.scope
+      const fs = yield* Effect.serviceOption(FSUtil.Service)
       const builds = MutableHashMap.empty<Location.Ref, { close?: Effect.Effect<void> }>()
       const inner: LayerMap.LayerMap<Location.Ref, LocationServices> = yield* LayerMap.make(
         (ref: Location.Ref) => {
@@ -24,7 +39,10 @@ export function buildLocationServiceMap(
           MutableHashMap.set(builds, ref, build)
           return Layer.fromBuild((memoMap, scope) =>
             Effect.suspend(() =>
-              Layer.buildWithMemoMap(Instance.layer(ref, { replacements: bindings }), memoMap, scope),
+              (ref.workspaceID || Option.isNone(fs) ? Effect.void : checkDirectory(fs.value, ref)).pipe(
+                Effect.orDie,
+                Effect.andThen(Layer.buildWithMemoMap(Instance.layer(ref, { replacements: bindings }), memoMap, scope)),
+              ),
             ).pipe(
               Effect.onExit((exit) => {
                 const finish = Effect.suspend(() => {
@@ -52,8 +70,7 @@ export function buildLocationServiceMap(
             ),
           )
         },
-        // Retain healthy graphs. Boot failures, not local filesystem probes,
-        // decide whether a location (including workspace placement) can retry.
+        // Retain healthy graphs; failed checks and boot failures retry on the next use.
         { idleTimeToLive: Duration.infinity },
       )
       const map = {
@@ -86,3 +103,26 @@ export function buildLocationServiceMap(
     }),
   )
 }
+
+function checkDirectory(fs: FSUtil.Interface, ref: Location.Ref) {
+  return fs.realPath(ref.directory).pipe(
+    Effect.asVoid,
+    Effect.catchReason("PlatformError", "NotFound", () => Effect.fail(new DirectoryNotFoundError(ref.directory))),
+    Effect.catchTag("PlatformError", (error) =>
+      isPermissionDenied(error) ? Effect.fail(new PermissionDeniedError(ref.directory)) : Effect.die(error),
+    ),
+  )
+}
+
+// Effect maps EACCES to PermissionDenied, but macOS privacy blocks report EPERM as Unknown.
+export function isPermissionDenied(error: PlatformError) {
+  if (error.reason._tag === "PermissionDenied") return true
+  const cause = error.cause
+  return (
+    error.reason._tag === "Unknown" &&
+    typeof cause === "object" &&
+    cause !== null &&
+    "code" in cause &&
+    cause.code === "EPERM"
+  )
+}
diff --git a/packages/server/src/location.ts b/packages/server/src/location.ts
index 05b52b956704..0bf98b1227a7 100644
--- a/packages/server/src/location.ts
+++ b/packages/server/src/location.ts
@@ -1,10 +1,12 @@
 import { Location } from "@opencode/core/location"
-import { LocationServiceMap } from "@opencode/core/location-services"
+import { DirectoryNotFoundError, LocationServiceMap, PermissionDeniedError } from "@opencode/core/location-services"
 import { AbsolutePath } from "@opencode/core/schema"
 import { Session } from "@opencode/core/session"
-import { InvalidRequestError, LocationDirectoryNotFoundError, LocationPermissionDeniedError } from "@opencode/protocol/errors"
-import { FSUtil } from "@opencode/util/fs-util"
-import type { PlatformError } from "effect/PlatformError"
+import {
+  InvalidRequestError,
+  LocationDirectoryNotFoundError,
+  LocationPermissionDeniedError,
+} from "@opencode/protocol/errors"
 import { Effect, Layer, Schema } from "effect"
 import { HttpServerRequest } from "effect/unstable/http"
 import { HttpApiMiddleware } from "effect/unstable/httpapi"
@@ -12,10 +14,10 @@ import { missingSession } from "./handlers/session-error"
 
 export type LocationServices = Layer.Success<ReturnType<(typeof LocationServiceMap.Service)["get"]>>
 
-export class LocationMiddleware extends HttpApiMiddleware.Service<
-  LocationMiddleware,
-  { provides: LocationServices }
->()("@opencode/HttpApiLocation", { error: [LocationDirectoryNotFoundError, LocationPermissionDeniedError] }) {}
+export class LocationMiddleware extends HttpApiMiddleware.Service<LocationMiddleware, { provides: LocationServices }>()(
+  "@opencode/HttpApiLocation",
+  { error: [LocationDirectoryNotFoundError, LocationPermissionDeniedError] },
+) {}
 
 export function response<A, E, R>(data: Effect.Effect<A, E, R>) {
   return Effect.gen(function* () {
@@ -57,58 +59,28 @@ function decode(input: string) {
   }
 }
 
-export const layer = (directoryCheck = true) =>
-  Layer.effect(
-    LocationMiddleware,
-    Effect.gen(function* () {
-      const locations = yield* LocationServiceMap.Service
-      const fs = yield* FSUtil.Service
-      return LocationMiddleware.of((effect) =>
-        Effect.gen(function* () {
-          const request = yield* HttpServerRequest.HttpServerRequest
-          const ref = requestRef(request)
-          // Resolve once before booting the Location graph; otherwise both a missing folder and
-          // macOS privacy denial become defects during Project/FileSystem startup.
-          if (directoryCheck)
-            yield* fs.realPath(ref.directory).pipe(
-              Effect.catchReason(
-                "PlatformError",
-                "NotFound",
-                () =>
-                  Effect.fail(
-                    new LocationDirectoryNotFoundError({
-                      directory: ref.directory,
-                      message: `Project directory not found: ${ref.directory}`,
-                    }),
-                  ),
-              ),
-              Effect.catchTag("PlatformError", (error) => {
-                if (isPermissionDenied(error))
-                  return Effect.fail(
-                    new LocationPermissionDeniedError({
-                      directory: ref.directory,
-                      message: `Cannot access project directory: ${ref.directory}`,
-                    }),
-                  )
-                return Effect.die(error)
-              }),
-            )
-          return yield* effect.pipe(Effect.provide(locations.get(ref)))
-        }),
-      )
-    }),
-  )
+export const layer = Layer.effect(
+  LocationMiddleware,
+  Effect.gen(function* () {
+    const locations = yield* LocationServiceMap.Service
+    return LocationMiddleware.of((effect) =>
+      Effect.gen(function* () {
+        const request = yield* HttpServerRequest.HttpServerRequest
+        return yield* effect.pipe(
+          Effect.provide(locations.get(requestRef(request))),
+          Effect.catchDefect(locationFailure),
+        )
+      }),
+    )
+  }),
+)
 
-// Effect maps EACCES to PermissionDenied but leaves EPERM as Unknown, which is how macOS reports a
-// folder blocked by privacy settings (e.g. `EPERM: operation not permitted, lstat '/Users/<user>/Documents'`).
-export function isPermissionDenied(error: PlatformError) {
-  if (error.reason._tag === "PermissionDenied") return true
-  const cause = error.cause
-  return (
-    error.reason._tag === "Unknown" &&
-    typeof cause === "object" &&
-    cause !== null &&
-    "code" in cause &&
-    cause.code === "EPERM"
-  )
+export function locationFailure(
+  defect: unknown,
+): Effect.Effect<never, LocationDirectoryNotFoundError | LocationPermissionDeniedError> {
+  if (defect instanceof DirectoryNotFoundError)
+    return Effect.fail(new LocationDirectoryNotFoundError({ directory: defect.directory, message: defect.message }))
+  if (defect instanceof PermissionDeniedError)
+    return Effect.fail(new LocationPermissionDeniedError({ directory: defect.directory, message: defect.message }))
+  return Effect.die(defect)
 }
diff --git a/packages/server/src/middleware/form-location.ts b/packages/server/src/middleware/form-location.ts
index dc18de75fbda..fae264dde166 100644
--- a/packages/server/src/middleware/form-location.ts
+++ b/packages/server/src/middleware/form-location.ts
@@ -1,17 +1,22 @@
 import { Instance } from "@opencode/core/instance/service"
 import { LocationServiceMap } from "@opencode/core/location-services"
 import { Session } from "@opencode/core/session"
-import { InvalidRequestError, SessionNotFoundError } from "@opencode/protocol/errors"
+import {
+  InvalidRequestError,
+  LocationDirectoryNotFoundError,
+  LocationPermissionDeniedError,
+  SessionNotFoundError,
+} from "@opencode/protocol/errors"
 import { Effect, Layer } from "effect"
 import { HttpRouter, HttpServerRequest } from "effect/unstable/http"
 import { HttpApiMiddleware } from "effect/unstable/httpapi"
-import { requestRef, sessionInfo, type LocationServices } from "../location"
+import { locationFailure, requestRef, sessionInfo, type LocationServices } from "../location"
 
 export class FormLocationMiddleware extends HttpApiMiddleware.Service<
   FormLocationMiddleware,
   { provides: LocationServices }
 >()("@opencode/HttpApiFormLocation", {
-  error: [InvalidRequestError, SessionNotFoundError],
+  error: [InvalidRequestError, SessionNotFoundError, LocationDirectoryNotFoundError, LocationPermissionDeniedError],
 }) {}
 
 export const formLocationLayer = Layer.effect(
@@ -34,7 +39,7 @@ export const formLocationLayer = Layer.effect(
 
         const session = yield* sessionInfo(sessions, route.params.sessionID)
         return yield* effect.pipe(instances.provide(session))
-      }),
+      }).pipe(Effect.catchDefect(locationFailure)),
     )
   }),
 )
diff --git a/packages/server/src/middleware/session-location.ts b/packages/server/src/middleware/session-location.ts
index f3a9a2234483..49d7e8e151bd 100644
--- a/packages/server/src/middleware/session-location.ts
+++ b/packages/server/src/middleware/session-location.ts
@@ -3,14 +3,19 @@ import { Session } from "@opencode/core/session"
 import { Effect, Layer } from "effect"
 import { HttpRouter } from "effect/unstable/http"
 import { HttpApiMiddleware } from "effect/unstable/httpapi"
-import { InvalidRequestError, SessionNotFoundError } from "@opencode/protocol/errors"
-import { sessionInfo, type LocationServices } from "../location"
+import {
+  InvalidRequestError,
+  LocationDirectoryNotFoundError,
+  LocationPermissionDeniedError,
+  SessionNotFoundError,
+} from "@opencode/protocol/errors"
+import { locationFailure, sessionInfo, type LocationServices } from "../location"
 
 export class SessionLocationMiddleware extends HttpApiMiddleware.Service<
   SessionLocationMiddleware,
   { provides: LocationServices }
 >()("@opencode/HttpApiSessionLocation", {
-  error: [InvalidRequestError, SessionNotFoundError],
+  error: [InvalidRequestError, SessionNotFoundError, LocationDirectoryNotFoundError, LocationPermissionDeniedError],
 }) {}
 
 export const sessionLocationLayer = Layer.effect(
@@ -24,7 +29,7 @@ export const sessionLocationLayer = Layer.effect(
         const route = yield* HttpRouter.RouteContext
         const session = yield* sessionInfo(sessions, route.params.sessionID)
         return yield* effect.pipe(instances.provide(session))
-      }),
+      }).pipe(Effect.catchDefect(locationFailure)),
     )
   }),
 )
diff --git a/packages/server/src/options.ts b/packages/server/src/options.ts
index 77038e3f761a..489006a36233 100644
--- a/packages/server/src/options.ts
+++ b/packages/server/src/options.ts
@@ -41,8 +41,6 @@ export const ServerOptions = Schema.Struct({
     Schema.Struct({
       filewatcher: Schema.optional(Schema.Boolean),
       fff: Schema.optional(Schema.Boolean),
-      // Hosts without a local project filesystem (e.g. workerd) opt out of the request-time directory probe.
-      directoryCheck: Schema.optional(Schema.Boolean),
     }),
   ),
 })
diff --git a/packages/server/src/routes.ts b/packages/server/src/routes.ts
index c2245a4d9ffc..eea50e1f61e7 100644
--- a/packages/server/src/routes.ts
+++ b/packages/server/src/routes.ts
@@ -179,7 +179,7 @@ function makeRoutes<AuthError, AuthServices>(
         Layer.provide(handlers.pipe(Layer.provide(services), Layer.provide(Layer.succeed(CorsConfig, options)))),
         Layer.provide(formLocationLayer),
         Layer.provide(sessionLocationLayer),
-        Layer.provide(layer(options.fs?.directoryCheck !== false && !options.simulation)),
+        Layer.provide(layer),
         Layer.provide(authorizationLayer),
         Layer.provide(schemaErrorLayer),
         Layer.provide(auth),
diff --git a/packages/server/src/workerd.ts b/packages/server/src/workerd.ts
index bb3e3193a1a3..949ee3fd4d06 100644
--- a/packages/server/src/workerd.ts
+++ b/packages/server/src/workerd.ts
@@ -62,7 +62,7 @@ export function serverOptions(options: Options): ServerOptions {
   return {
     app: options.app,
     password: options.password,
-    fs: { filewatcher: false, fff: false, directoryCheck: false },
+    fs: { filewatcher: false, fff: false },
     // Durable event history is how a turn orphaned by eviction is recovered:
     // the boot-time resume replays it. A runtime that dies without teardown
     // cannot opt out of it, so this is not exposed as an option.
diff --git a/packages/server/test/fetch.test.ts b/packages/server/test/fetch.test.ts
index 9920673f4f30..171a510d50bb 100644
--- a/packages/server/test/fetch.test.ts
+++ b/packages/server/test/fetch.test.ts
@@ -5,7 +5,9 @@ import path from "node:path"
 import { Agent } from "@opencode/schema/agent"
 import { Integration } from "@opencode/schema/integration"
 import { ServerInfo } from "@opencode/protocol/groups/server"
-import { Effect, Schedule, Schema } from "effect"
+import { FSUtil } from "@opencode/util/fs-util"
+import { NodeFileSystem } from "@effect/platform-node"
+import { Context, Effect, Layer, Schedule, Schema } from "effect"
 import { tmpdir, tmpdirScoped } from "../../core/test/fixture/tmpdir"
 import { it } from "../../core/test/lib/effect"
 import { ServerFetch } from "../src/fetch"
@@ -105,7 +107,9 @@ it.live("serves the HttpApi and enforces Basic auth like the Node server", () =>
       ),
     )
     expect(response.status).toBe(200)
-    const body = yield* Effect.promise(() => response.json()).pipe(Effect.flatMap(Schema.decodeUnknownEffect(ServerInfo)))
+    const body = yield* Effect.promise(() => response.json()).pipe(
+      Effect.flatMap(Schema.decodeUnknownEffect(ServerInfo)),
+    )
     expect(body.version).toBe("test-version")
     expect(body.paths.tmp).toEndWith("opencode")
   }),
@@ -146,6 +150,49 @@ it.live("reports a missing project directory and recovers when it returns", () =
   }),
 )
 
+it.live("checks a directory once per location boot, not on every request", () =>
+  Effect.gen(function* () {
+    const directory = yield* tmpdirScoped()
+    const checked: string[] = []
+    const filesystem = FSUtil.layer.pipe(
+      Layer.provide(NodeFileSystem.layer),
+      Layer.flatMap((context) => {
+        const fs = Context.get(context, FSUtil.Service)
+        return Layer.succeed(
+          FSUtil.Service,
+          FSUtil.Service.of({
+            ...fs,
+            realPath: (input) => {
+              if (input === directory.path) checked.push(input)
+              return fs.realPath(input)
+            },
+          }),
+        )
+      }),
+    )
+    const handler = yield* ServerFetch.make(options, { overrides: [FSUtil.node.replace(filesystem)] })
+    const request = (endpoint: string, method = "GET") =>
+      handler(
+        new Request(`http://opencode.local${endpoint}`, {
+          method,
+          headers: { "x-opencode-directory": encodeURIComponent(directory.path) },
+        }),
+      )
+
+    expect((yield* Effect.promise(() => request("/api/location"))).status).toBe(200)
+    const afterBoot = checked.length
+    expect(afterBoot).toBeGreaterThan(0)
+    expect((yield* Effect.promise(() => request("/api/location"))).status).toBe(200)
+    expect(checked).toHaveLength(afterBoot)
+
+    expect((yield* Effect.promise(() => request("/api/location/reload", "POST"))).status).toBe(204)
+    const afterReload = checked.length
+    expect(afterReload).toBeGreaterThan(afterBoot)
+    expect((yield* Effect.promise(() => request("/api/location"))).status).toBe(200)
+    expect(checked).toHaveLength(afterReload)
+  }),
+)
+
 it.live("reports denied project access without breaking other locations", () =>
   Effect.gen(function* () {
     if (process.platform === "win32") return
diff --git a/packages/server/test/location-permission.test.ts b/packages/server/test/location-permission.test.ts
index 5bb43d15c857..4c27dfa0fb13 100644
--- a/packages/server/test/location-permission.test.ts
+++ b/packages/server/test/location-permission.test.ts
@@ -1,6 +1,6 @@
 import { expect, test } from "bun:test"
 import { PlatformError } from "effect"
-import { isPermissionDenied } from "../src/location"
+import { isPermissionDenied } from "../../core/src/location-services"
 
 // Reproduces the error macOS returns when privacy settings block a folder.
 const macPrivacyDenied = () =>