diff --git a/crates/file_finder/src/open_path_prompt.rs b/crates/file_finder/src/open_path_prompt.rs
index 3a6522f308..2628fe81ce 100644
--- a/crates/file_finder/src/open_path_prompt.rs
+++ b/crates/file_finder/src/open_path_prompt.rs
@@ -236,7 +236,12 @@ impl PickerDelegate for OpenPathDelegate {
         let Some(candidate) = directory_state.match_candidates.get(*m) else {
             return;
         };
-        let result = Path::new(&directory_state.path).join(&candidate.string);
+        let result = Path::new(
+            self.lister
+                .resolve_tilde(&directory_state.path, cx)
+                .as_ref(),
+        )
+        .join(&candidate.string);
         if let Some(tx) = self.tx.take() {
             tx.send(Some(vec![result])).ok();
         }
diff --git a/crates/project/src/project.rs b/crates/project/src/project.rs
index 7ef29926fd..981ee5da14 100644
--- a/crates/project/src/project.rs
+++ b/crates/project/src/project.rs
@@ -664,6 +664,14 @@ impl DirectoryLister {
         }
     }
 
+    pub fn resolve_tilde<'a>(&self, path: &'a String, cx: &AppContext) -> Cow<'a, str> {
+        if self.is_local(cx) {
+            shellexpand::tilde(path)
+        } else {
+            Cow::from(path)
+        }
+    }
+
     pub fn default_query(&self, cx: &mut AppContext) -> String {
         if let DirectoryLister::Project(project) = self {
             if let Some(worktree) = project.read(cx).visible_worktrees(cx).next() {