diff --git a/packages/app/src/components/directory-picker-domain.test.ts b/packages/app/src/components/directory-picker-domain.test.ts
index aeaaafde3ed1..242b9d60f61c 100644
--- a/packages/app/src/components/directory-picker-domain.test.ts
+++ b/packages/app/src/components/directory-picker-domain.test.ts
@@ -237,6 +237,47 @@ test("searches from an absolute root without a default base", async () => {
   expect(directories).toEqual(["/"])
 })
 
+test("retries a failed directory listing without reopening the picker", async () => {
+  let attempts = 0
+  const sdk = {
+    api: {
+      file: {
+        list: () => {
+          attempts++
+          if (attempts === 1) return Promise.reject(new Error("Permission denied"))
+          return Promise.resolve({ data: [{ path: "My project 日本語/", type: "directory" }] })
+        },
+      },
+    },
+  } as unknown as Parameters<typeof createDirectorySearch>[0]["sdk"]
+  const search = createDirectorySearch({ sdk, home: () => "/home/luke", base: () => "/home/luke" })
+
+  expect(await search("~/")).toEqual(["/home/luke"])
+  expect(await search("~/")).toEqual(["/home/luke", "/home/luke/My project 日本語"])
+  expect(await search("~/My")).toEqual(["/home/luke/My project 日本語"])
+  expect(attempts).toBe(2)
+})
+
+test("does not replace newer results when an earlier directory listing fails", async () => {
+  const pending = Promise.withResolvers<{ data: { path: string; type: string }[] }>()
+  const sdk = {
+    api: {
+      file: {
+        list: (input: { location?: { directory?: string } }) =>
+          input.location?.directory === "/home/luke"
+            ? pending.promise
+            : Promise.resolve({ data: [{ path: "project/", type: "directory" }] }),
+      },
+    },
+  } as unknown as Parameters<typeof createDirectorySearch>[0]["sdk"]
+  const search = createDirectorySearch({ sdk, home: () => "/home/luke", base: () => "/home/luke" })
+
+  const previous = search("~/")
+  expect(await search("/project")).toEqual(["/project", "/project/project"])
+  pending.reject(new Error("Disconnected"))
+  expect(await previous).toEqual([])
+})
+
 test("identifies the next directory level to preload", () => {
   expect(
     preloadTreeDirectories("src/", [
diff --git a/packages/app/src/components/directory-picker-domain.ts b/packages/app/src/components/directory-picker-domain.ts
index dfd8ee74addc..628c20f75375 100644
--- a/packages/app/src/components/directory-picker-domain.ts
+++ b/packages/app/src/components/directory-picker-domain.ts
@@ -345,7 +345,10 @@ export function createDirectorySearch(args: { sdk: ServerSDK; base: () => string
     const request = args.sdk.api.file
       .list({ location: { directory: key } })
       .then((result) => result.data)
-      .catch(() => [])
+      .catch(() => {
+        cache.delete(key)
+        return []
+      })
       .then((nodes) =>
         nodes
           .filter((node) => node.type === "directory")