diff --git a/crates/agent_ui/Cargo.toml b/crates/agent_ui/Cargo.toml
index fcb23fd17f..03cb331334 100644
--- a/crates/agent_ui/Cargo.toml
+++ b/crates/agent_ui/Cargo.toml
@@ -145,3 +145,4 @@ tempfile.workspace = true
 vim.workspace = true
 tree-sitter-md.workspace = true
 unindent.workspace = true
+terminal = { workspace = true, features = ["test-support"] }
diff --git a/crates/agent_ui/src/agent_panel.rs b/crates/agent_ui/src/agent_panel.rs
index 4cab8aee37..88c5baa2b2 100644
--- a/crates/agent_ui/src/agent_panel.rs
+++ b/crates/agent_ui/src/agent_panel.rs
@@ -4905,32 +4905,79 @@ impl AgentPanel {
                 }),
             )
             .on_drop(cx.listener(move |this, paths: &ExternalPaths, window, cx| {
-                let tasks = paths
-                    .paths()
-                    .iter()
-                    .map(|path| {
-                        Workspace::project_path_for_path(this.project.clone(), path, false, cx)
-                    })
-                    .collect::<Vec<_>>();
-                cx.spawn_in(window, async move |this, cx| {
-                    let mut paths = vec![];
-                    let mut added_worktrees = vec![];
-                    let opened_paths = futures::future::join_all(tasks).await;
-                    for entry in opened_paths {
-                        if let Some((worktree, project_path)) = entry.log_err() {
-                            added_worktrees.push(worktree);
-                            paths.push(project_path);
-                        }
-                    }
-                    this.update_in(cx, |this, window, cx| {
-                        this.handle_drop(paths, added_worktrees, window, cx);
-                    })
-                    .ok();
-                })
-                .detach();
+                this.handle_external_paths_drop(paths, window, cx);
             }))
     }
 
+    fn handle_external_paths_drop(
+        &mut self,
+        paths: &ExternalPaths,
+        window: &mut Window,
+        cx: &mut Context<Self>,
+    ) {
+        if matches!(&self.base_view, BaseView::Terminal { .. }) {
+            // Terminal drops should match normal terminal views by pasting raw OS paths.
+            // The agent-thread path below converts paths to project paths, which can add
+            // worktrees and is only needed when attaching files to a conversation.
+            self.paste_external_paths_into_active_terminal(paths, window, cx);
+            return;
+        }
+
+        let BaseView::AgentThread { conversation_view } = &self.base_view else {
+            return;
+        };
+        let conversation_view = conversation_view.clone();
+        let tasks = paths
+            .paths()
+            .iter()
+            .map(|path| Workspace::project_path_for_path(self.project.clone(), path, false, cx))
+            .collect::<Vec<_>>();
+        cx.spawn_in(window, async move |_this, cx| {
+            let mut paths = vec![];
+            let mut added_worktrees = vec![];
+            let opened_paths = futures::future::join_all(tasks).await;
+            for entry in opened_paths {
+                if let Some((worktree, project_path)) = entry.log_err() {
+                    added_worktrees.push(worktree);
+                    paths.push(project_path);
+                }
+            }
+            conversation_view
+                .update_in(cx, |conversation_view, window, cx| {
+                    conversation_view.insert_dragged_files(paths, added_worktrees, window, cx);
+                })
+                .log_err();
+        })
+        .detach();
+    }
+
+    fn paste_external_paths_into_active_terminal(
+        &mut self,
+        paths: &ExternalPaths,
+        window: &mut Window,
+        cx: &mut Context<Self>,
+    ) {
+        let BaseView::Terminal { terminal_id } = &self.base_view else {
+            return;
+        };
+
+        if !self.project.read(cx).is_local() {
+            return;
+        }
+
+        let Some(terminal_view) = self
+            .terminals
+            .get(terminal_id)
+            .map(|terminal| terminal.view.clone())
+        else {
+            return;
+        };
+
+        terminal_view.update(cx, |terminal_view, cx| {
+            terminal_view.add_paths_to_terminal(paths.paths(), window, cx);
+        });
+    }
+
     fn handle_drop(
         &mut self,
         paths: Vec<ProjectPath>,
@@ -4944,7 +4991,30 @@ impl AgentPanel {
                     conversation_view.insert_dragged_files(paths, added_worktrees, window, cx);
                 });
             }
-            BaseView::Terminal { .. } | BaseView::Uninitialized => {}
+            BaseView::Terminal { terminal_id } => {
+                let paths = {
+                    let project = self.project.read(cx);
+                    paths
+                        .iter()
+                        .filter_map(|project_path| project.absolute_path(project_path, cx))
+                        .collect::<Vec<_>>()
+                };
+
+                if paths.is_empty() {
+                    return;
+                }
+
+                if let Some(terminal_view) = self
+                    .terminals
+                    .get(terminal_id)
+                    .map(|terminal| terminal.view.clone())
+                {
+                    terminal_view.update(cx, |terminal_view, cx| {
+                        terminal_view.add_paths_to_terminal(&paths, window, cx);
+                    });
+                }
+            }
+            BaseView::Uninitialized => {}
         }
     }
 
@@ -5003,7 +5073,9 @@ impl Render for AgentPanel {
                 VisibleSurface::AgentThread(conversation_view) => parent
                     .child(conversation_view.clone())
                     .child(self.render_drag_target(cx)),
-                VisibleSurface::Terminal(terminal_view) => parent.child(terminal_view.clone()),
+                VisibleSurface::Terminal(terminal_view) => parent
+                    .child(terminal_view.clone())
+                    .child(self.render_drag_target(cx)),
                 VisibleSurface::Configuration(configuration) => {
                     parent.children(configuration.cloned())
                 }
@@ -5279,7 +5351,7 @@ mod tests {
     use std::any::Any;
 
     use serde_json::json;
-    use std::path::Path;
+    use std::path::{Path, PathBuf};
     use std::sync::Arc;
     use std::time::Instant;
 
@@ -6669,6 +6741,175 @@ mod tests {
         (panel, cx)
     }
 
+    fn expected_terminal_drop_text(paths: &[PathBuf]) -> String {
+        let mut text = String::new();
+        for path in paths {
+            text.push(' ');
+            text.push_str(&format!("{path:?}"));
+        }
+        text.push(' ');
+        text
+    }
+
+    #[gpui::test]
+    async fn test_terminal_external_image_drop_writes_path(cx: &mut TestAppContext) {
+        let (panel, mut cx) = setup_panel(cx).await;
+        cx.update(|_, cx| {
+            cx.update_flags(true, vec!["agent-panel-terminal".to_string()]);
+        });
+
+        let terminal_id = panel
+            .update_in(&mut cx, |panel, window, cx| {
+                panel.insert_test_terminal("Image Upload", true, window, cx)
+            })
+            .expect("test terminal should be inserted");
+        cx.run_until_parked();
+
+        let terminal = panel.read_with(&cx, |panel, cx| {
+            panel
+                .terminals
+                .get(&terminal_id)
+                .expect("terminal should remain in the panel")
+                .view
+                .read(cx)
+                .terminal()
+                .clone()
+        });
+        terminal.update(&mut cx, |terminal, _cx| terminal.take_input_log());
+
+        let image_path = PathBuf::from("/tmp/dropped-image.png");
+        panel.update_in(&mut cx, |panel, window, cx| {
+            let external_paths = ExternalPaths(vec![image_path.clone()].into());
+            panel.paste_external_paths_into_active_terminal(&external_paths, window, cx);
+        });
+
+        let mut input_log = terminal.update(&mut cx, |terminal, _cx| terminal.take_input_log());
+        assert_eq!(input_log.len(), 1, "expected one write to the terminal");
+        let written =
+            String::from_utf8(input_log.remove(0)).expect("terminal write should be valid UTF-8");
+        assert_eq!(
+            written,
+            expected_terminal_drop_text(std::slice::from_ref(&image_path))
+        );
+    }
+
+    #[gpui::test]
+    async fn test_terminal_external_paths_drop_handler_writes_image_path(cx: &mut TestAppContext) {
+        let (panel, mut cx) = setup_panel(cx).await;
+        cx.update(|_, cx| {
+            cx.update_flags(true, vec!["agent-panel-terminal".to_string()]);
+        });
+
+        let terminal_id = panel
+            .update_in(&mut cx, |panel, window, cx| {
+                panel.insert_test_terminal("Image Upload", true, window, cx)
+            })
+            .expect("test terminal should be inserted");
+        cx.run_until_parked();
+
+        let terminal = panel.read_with(&cx, |panel, cx| {
+            panel
+                .terminals
+                .get(&terminal_id)
+                .expect("terminal should remain in the panel")
+                .view
+                .read(cx)
+                .terminal()
+                .clone()
+        });
+        terminal.update(&mut cx, |terminal, _cx| terminal.take_input_log());
+
+        let image_path = PathBuf::from("/tmp/dropped-image.png");
+        panel.update_in(&mut cx, |panel, window, cx| {
+            let external_paths = ExternalPaths(vec![image_path.clone()].into());
+            panel.handle_external_paths_drop(&external_paths, window, cx);
+        });
+
+        let mut input_log = terminal.update(&mut cx, |terminal, _cx| terminal.take_input_log());
+        assert_eq!(input_log.len(), 1, "expected one write to the terminal");
+        let written =
+            String::from_utf8(input_log.remove(0)).expect("terminal write should be valid UTF-8");
+        assert_eq!(
+            written,
+            expected_terminal_drop_text(std::slice::from_ref(&image_path))
+        );
+    }
+
+    #[gpui::test]
+    async fn test_external_file_drop_on_thread_does_not_paste_into_later_terminal(
+        cx: &mut TestAppContext,
+    ) {
+        init_test(cx);
+        cx.update(|cx| {
+            agent::ThreadStore::init_global(cx);
+            language_model::LanguageModelRegistry::test(cx);
+            cx.update_flags(true, vec!["agent-panel-terminal".to_string()]);
+        });
+
+        let fs = FakeFs::new(cx.executor());
+        cx.update(|cx| <dyn fs::Fs>::set_global(fs.clone(), cx));
+        fs.insert_tree("/project", json!({ "file.txt": "content" }))
+            .await;
+        let project = Project::test(fs.clone(), [Path::new("/project")], cx).await;
+
+        let multi_workspace =
+            cx.add_window(|window, cx| MultiWorkspace::test_new(project.clone(), window, cx));
+        let workspace = multi_workspace
+            .read_with(cx, |multi_workspace, _cx| {
+                multi_workspace.workspace().clone()
+            })
+            .unwrap();
+        let mut cx = VisualTestContext::from_window(multi_workspace.into(), cx);
+
+        let panel = workspace.update_in(&mut cx, |workspace, window, cx| {
+            let panel = cx.new(|cx| AgentPanel::new(workspace, None, window, cx));
+            workspace.add_panel(panel.clone(), window, cx);
+            panel
+        });
+        open_thread_with_connection(&panel, StubAgentConnection::new(), &mut cx);
+        let thread_id = active_thread_id(&panel, &cx);
+
+        let file_path = PathBuf::from("/project/file.txt");
+        panel.update_in(&mut cx, |panel, window, cx| {
+            let external_paths = ExternalPaths(vec![file_path.clone()].into());
+            panel.handle_external_paths_drop(&external_paths, window, cx);
+        });
+
+        let terminal_id = panel
+            .update_in(&mut cx, |panel, window, cx| {
+                panel.insert_test_terminal("Drop Target", true, window, cx)
+            })
+            .expect("test terminal should be inserted");
+        let terminal = panel.read_with(&cx, |panel, cx| {
+            panel
+                .terminals
+                .get(&terminal_id)
+                .expect("terminal should remain in the panel")
+                .view
+                .read(cx)
+                .terminal()
+                .clone()
+        });
+        terminal.update(&mut cx, |terminal, _cx| terminal.take_input_log());
+
+        cx.run_until_parked();
+
+        let input_log = terminal.update(&mut cx, |terminal, _cx| terminal.take_input_log());
+        assert!(
+            input_log.is_empty(),
+            "thread drop completion should not write to the active terminal"
+        );
+
+        let expected_uri = MentionUri::File {
+            abs_path: file_path,
+        }
+        .to_uri()
+        .to_string();
+        let expected_text = format!("[@file.txt]({expected_uri}) ");
+        let actual_text = panel.read_with(&cx, |panel, cx| panel.editor_text(thread_id, cx));
+        assert_eq!(actual_text.as_deref(), Some(expected_text.as_str()));
+    }
+
     #[gpui::test]
     async fn test_terminal_entry_kind_controls_new_entry(cx: &mut TestAppContext) {
         let (panel, mut cx) = setup_panel(cx).await;
diff --git a/crates/terminal_view/src/terminal_view.rs b/crates/terminal_view/src/terminal_view.rs
index 449e1c67d7..55e6929d83 100644
--- a/crates/terminal_view/src/terminal_view.rs
+++ b/crates/terminal_view/src/terminal_view.rs
@@ -855,7 +855,7 @@ impl TerminalView {
         });
     }
 
-    fn add_paths_to_terminal(&self, paths: &[PathBuf], window: &mut Window, cx: &mut App) {
+    pub fn add_paths_to_terminal(&self, paths: &[PathBuf], window: &mut Window, cx: &mut App) {
         let mut text = paths.iter().map(|path| format!(" {path:?}")).join("");
         text.push(' ');
         window.focus(&self.focus_handle(cx), cx);