diff --git a/rust/connlib/clients/apple/src/lib.rs b/rust/connlib/clients/apple/src/lib.rs
index 0b9e8f86a..76918430b 100644
--- a/rust/connlib/clients/apple/src/lib.rs
+++ b/rust/connlib/clients/apple/src/lib.rs
@@ -88,6 +88,7 @@ mod ffi {
             &self,
             tunnelAddressIPv4: String,
             tunnelAddressIPv6: String,
+            searchDomain: Option<String>,
             dnsAddresses: String,
             routeListv4: String,
             routeListv6: String,
@@ -128,7 +129,7 @@ impl Callbacks for CallbackHandler {
         tunnel_address_v4: Ipv4Addr,
         tunnel_address_v6: Ipv6Addr,
         dns_addresses: Vec<IpAddr>,
-        _search_domain: Option<DomainName>,
+        search_domain: Option<DomainName>,
         route_list_v4: Vec<Ipv4Network>,
         route_list_v6: Vec<Ipv6Network>,
     ) {
@@ -141,6 +142,7 @@ impl Callbacks for CallbackHandler {
                 self.inner.on_set_interface_config(
                     tunnel_address_v4.to_string(),
                     tunnel_address_v6.to_string(),
+                    search_domain.map(|s| s.to_string()),
                     dns_addresses,
                     route_list_4,
                     route_list_6,
diff --git a/swift/apple/FirezoneNetworkExtension/Adapter.swift b/swift/apple/FirezoneNetworkExtension/Adapter.swift
index 1d34f638e..1320fd8ea 100644
--- a/swift/apple/FirezoneNetworkExtension/Adapter.swift
+++ b/swift/apple/FirezoneNetworkExtension/Adapter.swift
@@ -363,6 +363,7 @@ extension Adapter: CallbackHandlerDelegate {
   public func onSetInterfaceConfig(
     tunnelAddressIPv4: String,
     tunnelAddressIPv6: String,
+    searchDomain: String?,
     dnsAddresses: [String],
     routeListv4: String,
     routeListv6: String
@@ -393,6 +394,7 @@ extension Adapter: CallbackHandlerDelegate {
       networkSettings.dnsAddresses = dnsAddresses
       networkSettings.routes4 = routes4
       networkSettings.routes6 = routes6
+      networkSettings.setSearchDomain(domain: searchDomain)
 
       networkSettings.apply()
     }
@@ -474,7 +476,7 @@ extension Adapter {
     let semaphore = DispatchSemaphore(value: 0)
 
     // Set tunnel's matchDomains to a dummy string that will never match any name
-    networkSettings.matchDomains = ["firezone-fd0020211111"]
+    networkSettings.setDummyMatchDomain()
 
     // Call apply to populate /etc/resolv.conf with the system's default resolvers
     networkSettings.apply {
@@ -484,7 +486,7 @@ extension Adapter {
       resolvers = BindResolvers().getservers().map(BindResolvers.getnameinfo)
 
       // Restore connlib's DNS resolvers
-      networkSettings.matchDomains = [""]
+      networkSettings.clearDummyMatchDomain()
       networkSettings.apply { semaphore.signal() }
     }
 
diff --git a/swift/apple/FirezoneNetworkExtension/CallbackHandler.swift b/swift/apple/FirezoneNetworkExtension/CallbackHandler.swift
index 5ba9f458e..431720583 100644
--- a/swift/apple/FirezoneNetworkExtension/CallbackHandler.swift
+++ b/swift/apple/FirezoneNetworkExtension/CallbackHandler.swift
@@ -20,6 +20,7 @@ public protocol CallbackHandlerDelegate: AnyObject {
   func onSetInterfaceConfig(
     tunnelAddressIPv4: String,
     tunnelAddressIPv6: String,
+    searchDomain: String?,
     dnsAddresses: [String],
     routeListv4: String,
     routeListv6: String
@@ -34,6 +35,7 @@ public class CallbackHandler {
   func onSetInterfaceConfig(
     tunnelAddressIPv4: RustString,
     tunnelAddressIPv6: RustString,
+    searchDomain: RustString?,
     dnsAddresses: RustString,
     routeListv4: RustString,
     routeListv6: RustString
@@ -43,6 +45,7 @@ public class CallbackHandler {
         CallbackHandler.onSetInterfaceConfig:
           IPv4: \(tunnelAddressIPv4.toString())
           IPv6: \(tunnelAddressIPv6.toString())
+          SearchDomain: \(String(describing: (searchDomain?.toString())))
           DNS: \(dnsAddresses.toString())
           IPv4 routes:  \(routeListv4.toString())
           IPv6 routes: \(routeListv6.toString())
@@ -57,6 +60,7 @@ public class CallbackHandler {
     delegate?.onSetInterfaceConfig(
       tunnelAddressIPv4: tunnelAddressIPv4.toString(),
       tunnelAddressIPv6: tunnelAddressIPv6.toString(),
+      searchDomain: searchDomain?.toString(),
       dnsAddresses: dnsArray,
       routeListv4: routeListv4.toString(),
       routeListv6: routeListv6.toString()
diff --git a/swift/apple/FirezoneNetworkExtension/Connlib/Generated/connlib-client-apple/connlib-client-apple.swift b/swift/apple/FirezoneNetworkExtension/Connlib/Generated/connlib-client-apple/connlib-client-apple.swift
index 39bb89c88..797a13206 100644
--- a/swift/apple/FirezoneNetworkExtension/Connlib/Generated/connlib-client-apple/connlib-client-apple.swift
+++ b/swift/apple/FirezoneNetworkExtension/Connlib/Generated/connlib-client-apple/connlib-client-apple.swift
@@ -1,6 +1,6 @@
 @_cdecl("__swift_bridge__$CallbackHandler$on_set_interface_config")
-func __swift_bridge__CallbackHandler_on_set_interface_config (_ this: UnsafeMutableRawPointer, _ tunnelAddressIPv4: UnsafeMutableRawPointer, _ tunnelAddressIPv6: UnsafeMutableRawPointer, _ dnsAddresses: UnsafeMutableRawPointer, _ routeListv4: UnsafeMutableRawPointer, _ routeListv6: UnsafeMutableRawPointer) {
-    Unmanaged<CallbackHandler>.fromOpaque(this).takeUnretainedValue().onSetInterfaceConfig(tunnelAddressIPv4: RustString(ptr: tunnelAddressIPv4), tunnelAddressIPv6: RustString(ptr: tunnelAddressIPv6), dnsAddresses: RustString(ptr: dnsAddresses), routeListv4: RustString(ptr: routeListv4), routeListv6: RustString(ptr: routeListv6))
+func __swift_bridge__CallbackHandler_on_set_interface_config (_ this: UnsafeMutableRawPointer, _ tunnelAddressIPv4: UnsafeMutableRawPointer, _ tunnelAddressIPv6: UnsafeMutableRawPointer, _ searchDomain: UnsafeMutableRawPointer?, _ dnsAddresses: UnsafeMutableRawPointer, _ routeListv4: UnsafeMutableRawPointer, _ routeListv6: UnsafeMutableRawPointer) {
+    Unmanaged<CallbackHandler>.fromOpaque(this).takeUnretainedValue().onSetInterfaceConfig(tunnelAddressIPv4: RustString(ptr: tunnelAddressIPv4), tunnelAddressIPv6: RustString(ptr: tunnelAddressIPv6), searchDomain: { let val = searchDomain; if val != nil { return RustString(ptr: val!) } else { return nil } }(), dnsAddresses: RustString(ptr: dnsAddresses), routeListv4: RustString(ptr: routeListv4), routeListv6: RustString(ptr: routeListv6))
 }
 
 @_cdecl("__swift_bridge__$CallbackHandler$on_update_resources")
diff --git a/swift/apple/FirezoneNetworkExtension/NetworkSettings.swift b/swift/apple/FirezoneNetworkExtension/NetworkSettings.swift
index 51e5e0b4d..00174ee8c 100644
--- a/swift/apple/FirezoneNetworkExtension/NetworkSettings.swift
+++ b/swift/apple/FirezoneNetworkExtension/NetworkSettings.swift
@@ -23,12 +23,36 @@ class NetworkSettings {
   public var dnsAddresses: [String] = []
   public var routes4: [NEIPv4Route] = []
   public var routes6: [NEIPv6Route] = []
-  public var matchDomains: [String] = [""]
+
+  // Private to ensure we append the search domain if we set it.
+  private var matchDomains: [String] = [""]
+  private var searchDomains: [String] = [""]
 
   init(packetTunnelProvider: PacketTunnelProvider?) {
     self.packetTunnelProvider = packetTunnelProvider
   }
 
+  func setSearchDomain(domain: String?) {
+    guard let domain = domain else {
+        self.matchDomains = [""]
+        self.searchDomains = [""]
+        return;
+    }
+
+    self.matchDomains = ["", domain]
+    self.searchDomains = [domain]
+  }
+
+  func setDummyMatchDomain() {
+    self.matchDomains = ["firezone-fd0020211111"]
+  }
+
+  func clearDummyMatchDomain() {
+    self.matchDomains = [""]
+
+    self.matchDomains.append(contentsOf: self.searchDomains)
+  }
+
   func apply(completionHandler: (() -> Void)? = nil) {
     // We don't really know the connlib gateway IP address at this point, but just using 127.0.0.1 is okay
     // because the OS doesn't really need this IP address.
@@ -46,7 +70,8 @@ class NetworkSettings {
     ipv4Settings.includedRoutes = routes4
     ipv6Settings.includedRoutes = routes6
     dnsSettings.matchDomains = matchDomains
-    dnsSettings.matchDomainsNoSearch = true
+    dnsSettings.searchDomains = searchDomains
+    dnsSettings.matchDomainsNoSearch = false
     tunnelNetworkSettings.ipv4Settings = ipv4Settings
     tunnelNetworkSettings.ipv6Settings = ipv6Settings
     tunnelNetworkSettings.dnsSettings = dnsSettings