diff --git a/crates/agent_servers/src/acp.rs b/crates/agent_servers/src/acp.rs
index f7b6a59a63b02028a8b30c905c92b82805a52b33..5f452bc9c0e2e9c2322042583295894a5866b053 100644
--- a/crates/agent_servers/src/acp.rs
+++ b/crates/agent_servers/src/acp.rs
@@ -203,11 +203,15 @@ impl AcpConnection {
             builder.build_std_command(Some(command.path.display().to_string()), &command.args);
         child.envs(command.env.iter().flatten());
         if let Some(cwd) = project.update(cx, |project, cx| {
-            project
-                .default_path_list(cx)
-                .ordered_paths()
-                .next()
-                .cloned()
+            if project.is_local() {
+                project
+                    .default_path_list(cx)
+                    .ordered_paths()
+                    .next()
+                    .cloned()
+            } else {
+                None
+            }
         }) {
             child.current_dir(cwd);
         }
diff --git a/crates/project/src/agent_server_store.rs b/crates/project/src/agent_server_store.rs
index a9003e8567e6bf57ea18f8d70619e9417a626f43..ca80fb39a526e380f2c6e4abb6c3f728843df8ba 100644
--- a/crates/project/src/agent_server_store.rs
+++ b/crates/project/src/agent_server_store.rs
@@ -27,6 +27,8 @@ use util::{ResultExt as _, debug_panic};
 use crate::ProjectEnvironment;
 use crate::agent_registry_store::{AgentRegistryStore, RegistryAgent, RegistryTargetConfig};
 
+use crate::worktree_store::WorktreeStore;
+
 #[derive(Deserialize, Serialize, Clone, PartialEq, Eq, JsonSchema)]
 pub struct AgentServerCommand {
     #[serde(rename = "command")]
@@ -149,6 +151,7 @@ enum AgentServerStoreState {
     Remote {
         project_id: u64,
         upstream_client: Entity<RemoteClient>,
+        worktree_store: Entity<WorktreeStore>,
     },
     Collab,
 }
@@ -231,6 +234,7 @@ impl AgentServerStore {
             AgentServerStoreState::Remote {
                 project_id,
                 upstream_client,
+                worktree_store,
             } => {
                 let mut agents = vec![];
                 for (ext_id, manifest) in manifests {
@@ -256,6 +260,7 @@ impl AgentServerStore {
                                     Box::new(RemoteExternalAgentServer {
                                         project_id: *project_id,
                                         upstream_client: upstream_client.clone(),
+                                        worktree_store: worktree_store.clone(),
                                         name: agent_server_name.clone(),
                                         new_version_available_tx: None,
                                     })
@@ -612,11 +617,16 @@ impl AgentServerStore {
         this
     }
 
-    pub(crate) fn remote(project_id: u64, upstream_client: Entity<RemoteClient>) -> Self {
+    pub(crate) fn remote(
+        project_id: u64,
+        upstream_client: Entity<RemoteClient>,
+        worktree_store: Entity<WorktreeStore>,
+    ) -> Self {
         Self {
             state: AgentServerStoreState::Remote {
                 project_id,
                 upstream_client,
+                worktree_store,
             },
             external_agents: HashMap::default(),
         }
@@ -751,8 +761,10 @@ impl AgentServerStore {
                 .env
                 .map(|env| env.into_iter().collect())
                 .unwrap_or_default(),
-            // root_dir and login are no longer used, but returned for backwards compatibility
-            root_dir: paths::home_dir().to_string_lossy().to_string(),
+            root_dir: envelope
+                .payload
+                .root_dir
+                .unwrap_or_else(|| paths::home_dir().to_string_lossy().to_string()),
             login: None,
         })
     }
@@ -766,6 +778,7 @@ impl AgentServerStore {
             let AgentServerStoreState::Remote {
                 project_id,
                 upstream_client,
+                worktree_store,
             } = &this.state
             else {
                 debug_panic!(
@@ -810,6 +823,7 @@ impl AgentServerStore {
                     let agent = RemoteExternalAgentServer {
                         project_id: *project_id,
                         upstream_client: upstream_client.clone(),
+                        worktree_store: worktree_store.clone(),
                         name: agent_id.clone(),
                         new_version_available_tx: new_version_available_txs
                             .remove(&agent_id)
@@ -906,6 +920,7 @@ impl AgentServerStore {
 struct RemoteExternalAgentServer {
     project_id: u64,
     upstream_client: Entity<RemoteClient>,
+    worktree_store: Entity<WorktreeStore>,
     name: AgentId,
     new_version_available_tx: Option<watch::Sender<Option<String>>>,
 }
@@ -920,8 +935,16 @@ impl ExternalAgentServer for RemoteExternalAgentServer {
         let project_id = self.project_id;
         let name = self.name.to_string();
         let upstream_client = self.upstream_client.downgrade();
+        let worktree_store = self.worktree_store.clone();
         self.new_version_available_tx = new_version_available_tx;
         cx.spawn(async move |cx| {
+            let root_dir = worktree_store.read_with(cx, |worktree_store, cx| {
+                crate::Project::default_visible_worktree_paths(worktree_store, cx)
+                    .into_iter()
+                    .next()
+                    .map(|path| path.display().to_string())
+            });
+
             let mut response = upstream_client
                 .update(cx, |upstream_client, _| {
                     upstream_client
@@ -929,7 +952,7 @@ impl ExternalAgentServer for RemoteExternalAgentServer {
                         .request(proto::GetAgentServerCommand {
                             project_id,
                             name,
-                            root_dir: None,
+                            root_dir,
                         })
                 })?
                 .await?;
diff --git a/crates/project/src/project.rs b/crates/project/src/project.rs
index 68a383224bcbbe99a655ab020646d4135138f14e..3dbfc6edc6ef4b2d59e028d027ebc29fc5b9f0d0 100644
--- a/crates/project/src/project.rs
+++ b/crates/project/src/project.rs
@@ -1500,8 +1500,13 @@ impl Project {
                 )
             });
 
-            let agent_server_store =
-                cx.new(|_| AgentServerStore::remote(REMOTE_SERVER_PROJECT_ID, remote.clone()));
+            let agent_server_store = cx.new(|_| {
+                AgentServerStore::remote(
+                    REMOTE_SERVER_PROJECT_ID,
+                    remote.clone(),
+                    worktree_store.clone(),
+                )
+            });
 
             cx.subscribe(&remote, Self::on_remote_client_event).detach();
 
@@ -2294,8 +2299,11 @@ impl Project {
         self.worktree_store.read(cx).visible_worktrees(cx)
     }
 
-    pub fn default_path_list(&self, cx: &App) -> PathList {
-        let worktree_roots = self
+    pub(crate) fn default_visible_worktree_paths(
+        worktree_store: &WorktreeStore,
+        cx: &App,
+    ) -> Vec<PathBuf> {
+        worktree_store
             .visible_worktrees(cx)
             .sorted_by(|left, right| {
                 left.read(cx)
@@ -2311,7 +2319,12 @@ impl Project {
                     Some(path.to_path_buf())
                 }
             })
-            .collect::<Vec<_>>();
+            .collect()
+    }
+
+    pub fn default_path_list(&self, cx: &App) -> PathList {
+        let worktree_roots =
+            Self::default_visible_worktree_paths(&self.worktree_store.read(cx), cx);
 
         if worktree_roots.is_empty() {
             PathList::new(&[paths::home_dir().as_path()])