diff --git a/macos/Sources/Ghostty/Ghostty.Action.swift b/macos/Sources/Ghostty/Ghostty.Action.swift
index 9d389a8c2..8fce2199d 100644
--- a/macos/Sources/Ghostty/Ghostty.Action.swift
+++ b/macos/Sources/Ghostty/Ghostty.Action.swift
@@ -115,6 +115,18 @@ extension Ghostty.Action {
             len = c.len
         }
     }
+
+    struct StartSearch {
+        let needle: String?
+        
+        init(c: ghostty_action_start_search_s) {
+            if let needleCString = c.needle {
+                self.needle = String(cString: needleCString)
+            } else {
+                self.needle = nil
+            }
+        }
+    }
 }
 
 // Putting the initializer in an extension preserves the automatic one.
diff --git a/macos/Sources/Ghostty/Ghostty.App.swift b/macos/Sources/Ghostty/Ghostty.App.swift
index 9c19199e8..5c62e7040 100644
--- a/macos/Sources/Ghostty/Ghostty.App.swift
+++ b/macos/Sources/Ghostty/Ghostty.App.swift
@@ -606,6 +606,9 @@ extension Ghostty {
             case GHOSTTY_ACTION_CLOSE_ALL_WINDOWS:
                 closeAllWindows(app, target: target)
 
+            case GHOSTTY_ACTION_START_SEARCH:
+                startSearch(app, target: target, v: action.action.start_search)
+
             case GHOSTTY_ACTION_TOGGLE_TAB_OVERVIEW:
                 fallthrough
             case GHOSTTY_ACTION_TOGGLE_WINDOW_DECORATIONS:
@@ -1641,6 +1644,29 @@ extension Ghostty {
             }
         }
 
+        private static func startSearch(
+            _ app: ghostty_app_t,
+            target: ghostty_target_s,
+            v: ghostty_action_start_search_s) {
+            switch (target.tag) {
+            case GHOSTTY_TARGET_APP:
+                Ghostty.logger.warning("start_search does nothing with an app target")
+                return
+
+            case GHOSTTY_TARGET_SURFACE:
+                guard let surface = target.target.surface else { return }
+                guard let surfaceView = self.surfaceView(from: surface) else { return }
+
+                let startSearch = Ghostty.Action.StartSearch(c: v)
+                DispatchQueue.main.async {
+                    surfaceView.searchState = Ghostty.SurfaceView.SearchState(from: startSearch)
+                }
+
+            default:
+                assertionFailure()
+            }
+        }
+
         private static func configReload(
             _ app: ghostty_app_t,
             target: ghostty_target_s,
diff --git a/macos/Sources/Ghostty/SurfaceView.swift b/macos/Sources/Ghostty/SurfaceView.swift
index f7cc455fc..dabfb4a57 100644
--- a/macos/Sources/Ghostty/SurfaceView.swift
+++ b/macos/Sources/Ghostty/SurfaceView.swift
@@ -197,10 +197,12 @@ extension Ghostty {
                     SecureInputOverlay()
                 }
                 #endif
-                
+
                 // Search overlay
-                SurfaceSearchOverlay()
-                
+                if surfaceView.searchState != nil {
+                    SurfaceSearchOverlay(searchState: $surfaceView.searchState)
+                }
+
                 // Show bell border if enabled
                 if (ghostty.config.bellFeatures.contains(.border)) {
                     BellBorderOverlay(bell: surfaceView.bell)
@@ -387,10 +389,12 @@ extension Ghostty {
 
     /// Search overlay view that displays a search bar with input field and navigation buttons.
     struct SurfaceSearchOverlay: View {
+        @Binding var searchState: SurfaceView.SearchState?
         @State private var searchText: String = ""
         @State private var corner: Corner = .topRight
         @State private var dragOffset: CGSize = .zero
         @State private var barSize: CGSize = .zero
+        @FocusState private var isSearchFieldFocused: Bool
         
         private let padding: CGFloat = 8
         
@@ -404,6 +408,7 @@ extension Ghostty {
                         .padding(.vertical, 6)
                         .background(Color.primary.opacity(0.1))
                         .cornerRadius(6)
+                        .focused($isSearchFieldFocused)
                     
                     Button(action: {}) {
                         Image(systemName: "chevron.up")
@@ -415,7 +420,9 @@ extension Ghostty {
                     }
                     .buttonStyle(.borderless)
                     
-                    Button(action: {}) {
+                    Button(action: {
+                        searchState = nil
+                    }) {
                         Image(systemName: "xmark")
                     }
                     .buttonStyle(.borderless)
@@ -424,6 +431,12 @@ extension Ghostty {
                 .background(.background)
                 .cornerRadius(8)
                 .shadow(radius: 4)
+                .onAppear {
+                    if let needle = searchState?.needle {
+                        searchText = needle
+                    }
+                    isSearchFieldFocused = true
+                }
                 .background(
                     GeometryReader { barGeo in
                         Color.clear.onAppear {
@@ -770,3 +783,15 @@ extension FocusedValues {
         typealias Value = OSSize
     }
 }
+
+// MARK: Search State
+
+extension Ghostty.SurfaceView {
+    class SearchState: ObservableObject {
+        @Published var needle: String = ""
+
+        init(from startSearch: Ghostty.Action.StartSearch) {
+            self.needle = startSearch.needle ?? ""
+        }
+    }
+}
diff --git a/macos/Sources/Ghostty/SurfaceView_AppKit.swift b/macos/Sources/Ghostty/SurfaceView_AppKit.swift
index 6e3597fd3..19054b6c3 100644
--- a/macos/Sources/Ghostty/SurfaceView_AppKit.swift
+++ b/macos/Sources/Ghostty/SurfaceView_AppKit.swift
@@ -64,6 +64,9 @@ extension Ghostty {
         // The currently active key sequence. The sequence is not active if this is empty.
         @Published var keySequence: [KeyboardShortcut] = []
 
+        // The current search state. When non-nil, the search overlay should be shown.
+        @Published var searchState: SearchState? = nil
+
         // The time this surface last became focused. This is a ContinuousClock.Instant
         // on supported platforms.
         @Published var focusInstant: ContinuousClock.Instant? = nil