diff --git a/webviews/src/agent-session/acpmux/App.tsx b/webviews/src/agent-session/acpmux/App.tsx
index a2c062a1e8f9..49fe50dc1190 100644
--- a/webviews/src/agent-session/acpmux/App.tsx
+++ b/webviews/src/agent-session/acpmux/App.tsx
@@ -7814,9 +7814,11 @@ function AcpmuxPane({ initialChat }: { initialChat?: InitialChat }) {
   // so the client knows it as `local` (ownMachineFolders).
   const paneMachine =
     snapshot.summary?.peer || (snapshot.summary?.hostKind === "cloud" && snapshot.summary.host) || "local";
+  // Only a start here takes them: a Cloud or Sandboxed start carries no extra folders (cmux#34403).
+  const extraFoldersSent = sandbox.mode === "persistent" ? extraFolderDraft : undefined;
   useEffect(() => {
-    directClient.current?.setNewChatFolders(ownMachineFolders(extraFolderDraft, paneMachine));
-  }, [extraFolderDraft, paneMachine, clientEpoch]);
+    directClient.current?.setNewChatFolders(ownMachineFolders(extraFoldersSent, paneMachine));
+  }, [extraFoldersSent, paneMachine, clientEpoch]);
   const continuationProject = useRef(projectDraft);
   const continuationProjectGeneration = useRef(0);
   useLayoutEffect(() => {
diff --git a/webviews/src/agent-session/acpmux/ComposerContext.tsx b/webviews/src/agent-session/acpmux/ComposerContext.tsx
index cbf1ceb722cf..a3b2a9384ab7 100644
--- a/webviews/src/agent-session/acpmux/ComposerContext.tsx
+++ b/webviews/src/agent-session/acpmux/ComposerContext.tsx
@@ -507,6 +507,8 @@ export function ComposerContext({
   const pickCloudMachine = (id: string) => {
     const machine = computers.find((computer) => computer.id === id)?.cloudMachine;
     if (machine && !readOnly) {
+      // Folders are the machine's: the pick drops this machine's at once, not when (or if) it arrives (cmux#34527).
+      if (extraFolders?.draft) extraFolders.onChange(undefined);
       onCloudMachine(machine);
       setWaiting({ key: pickKey, id: machine.id, name: machine.name });
     }
@@ -579,7 +581,11 @@ export function ComposerContext({
   };
   const folderShown = !savedPick && !(readOnly && !newChats && !currentFolder);
   // The new chat's extra folders on the picked machine (a pick of the chat's own folder is never one).
-  const extraShown = extraFolders && !readOnly ? draftFolders(extraFolders.draft, selectedComputer) : undefined;
+  // A Cloud or Sandboxed start carries none (cmux#34403), so those modes offer no Add folder… or +N.
+  const extraShown =
+    extraFolders && !readOnly && !cloudPicked && !sandboxPicked
+      ? draftFolders(extraFolders.draft, selectedComputer)
+      : undefined;
   const extra: ExtraFolderRows | undefined =
     extraFolders && extraShown
       ? {
diff --git a/webviews/src/agent-session/acpmux/FolderPopover.tsx b/webviews/src/agent-session/acpmux/FolderPopover.tsx
index a2284071a1e4..f5050605de02 100644
--- a/webviews/src/agent-session/acpmux/FolderPopover.tsx
+++ b/webviews/src/agent-session/acpmux/FolderPopover.tsx
@@ -332,7 +332,12 @@ export function FolderPopover({
             close();
           } else {
             setOpen(next);
-            if (!next) setQuery("");
+            // Every close ends Add folder…'s mode, an outside click as much as Escape (cmux#34408).
+            if (!next) {
+              setQuery("");
+              setExpanded(new Set());
+              setAddingExtra(false);
+            }
           }
         }}
         anchor={open ? anchor : null}
diff --git a/webviews/test/composer-extra-folders.test.tsx b/webviews/test/composer-extra-folders.test.tsx
index 6cfd975839db..c788958a3168 100644
--- a/webviews/test/composer-extra-folders.test.tsx
+++ b/webviews/test/composer-extra-folders.test.tsx
@@ -165,3 +165,82 @@ test("a started chat offers no Add folder…", async () => {
     await act(async () => root.unmount());
   }
 });
+
+// cmux#34408: an outside dismiss after Add folder… ends add mode, so the next pick changes the project.
+test("an outside dismiss after Add folder… leaves the next pick changing the project", async () => {
+  const picked: string[] = [];
+  const { root, changes } = await renderTray({ onProject: (cwd: string) => picked.push(cwd) });
+  try {
+    await openFolderMenu();
+    await press(menuItem("Add folder…")!);
+    const outside = dom.window.document.body;
+    await act(async () => {
+      for (const type of ["pointerdown", "mousedown", "pointerup", "mouseup", "click"])
+        outside.dispatchEvent(new dom.window.MouseEvent(type, { bubbles: true, button: 0 }));
+    });
+    await settle();
+    expect(dom.window.document.querySelector(".acpmux-folder-popover")).toBeNull();
+    await openFolderMenu();
+    expect(menuItem("Add folder…")).toBeDefined();
+    await press(menuItem("notes")!);
+    expect(picked).toEqual(["/Users/me/notes"]);
+    expect(changes).toEqual([]);
+  } finally {
+    await act(async () => root.unmount());
+  }
+});
+
+// cmux#34403: Cloud and Sandboxed starts carry no extra folders, so the composer offers none.
+for (const mode of ["cloud", "sandboxed"] as const) {
+  test(`${mode} run mode offers no Add folder… and shows no +N`, async () => {
+    const { root } = await renderTray(
+      { runMode: { mode, onMode: () => {} } },
+      { machine: "local", folders: ["/Users/me/notes"] },
+    );
+    try {
+      expect(face()).not.toContain("+1");
+      await openFolderMenu();
+      expect(menuItem("Add folder…")).toBeUndefined();
+      expect(dom.window.document.querySelectorAll(".acpmux-extra-folder").length).toBe(0);
+    } finally {
+      await act(async () => root.unmount());
+    }
+  });
+}
+
+// cmux#34527: a pick of an account Cloud machine that is still starting drops this machine's folders
+// at once, not only once it arrives (or never, when it fails to start).
+test("picking a starting Cloud machine drops this machine's extra folders at once", async () => {
+  const cloud: string[] = [];
+  const { root, changes } = await renderTray(
+    {
+      sessions: [],
+      onConnect: () => undefined,
+      onCloudMachine: (machine: { id: string }) => cloud.push(machine.id),
+      cloudMachines: [{ id: "vm-ready", name: "eval box", stage: "ready" }],
+    },
+    { machine: "local", folders: ["/Users/me/notes"] },
+  );
+  try {
+    expect(face()).toContain("+1");
+    const machine = [...dom.window.document.querySelectorAll<HTMLButtonElement>(".acpmux-location-button")].find(
+      (button) => (button.getAttribute("aria-label") ?? "").includes(":"),
+    );
+    expect(machine).toBeDefined();
+    await act(async () => {
+      machine!.dispatchEvent(new dom.window.MouseEvent("pointerdown", { bubbles: true }));
+      machine!.click();
+    });
+    await settle();
+    const row = [...dom.window.document.querySelectorAll<HTMLElement>(".acpmux-location-menu .acpmux-menu-item")].find(
+      (item) => item.textContent?.includes("eval box"),
+    );
+    expect(row).toBeDefined();
+    await press(row!);
+    expect(cloud).toEqual(["vm-ready"]);
+    expect(changes.at(-1)).toBeUndefined();
+    expect(changes.length).toBe(1);
+  } finally {
+    await act(async () => root.unmount());
+  }
+});