diff --git a/mullvad-cli/src/cmds/relay.rs b/mullvad-cli/src/cmds/relay.rs
index cb4dca2b2d..36d2f51bd6 100644
--- a/mullvad-cli/src/cmds/relay.rs
+++ b/mullvad-cli/src/cmds/relay.rs
@@ -451,6 +451,7 @@ impl Relay {
                 exit_peer: None,
                 ipv4_gateway,
                 ipv6_gateway,
+                routes: None,
                 // NOTE: Ignored in gRPC
                 #[cfg(target_os = "linux")]
                 fwmark: None,
diff --git a/mullvad-daemon/src/tunnel.rs b/mullvad-daemon/src/tunnel.rs
index 0ca531189f..7a4938ea38 100644
--- a/mullvad-daemon/src/tunnel.rs
+++ b/mullvad-daemon/src/tunnel.rs
@@ -177,6 +177,7 @@ impl InnerParametersGenerator {
                 exit_peer: endpoint.exit_peer,
                 ipv4_gateway: endpoint.ipv4_gateway,
                 ipv6_gateway: Some(endpoint.ipv6_gateway),
+                routes: None,
                 #[cfg(target_os = "linux")]
                 fwmark: Some(mullvad_types::TUNNEL_FWMARK),
             },
diff --git a/mullvad-management-interface/src/types/conversions/custom_tunnel.rs b/mullvad-management-interface/src/types/conversions/custom_tunnel.rs
index 5b4ce004ec..1c2be5cfa4 100644
--- a/mullvad-management-interface/src/types/conversions/custom_tunnel.rs
+++ b/mullvad-management-interface/src/types/conversions/custom_tunnel.rs
@@ -73,6 +73,8 @@ impl TryFrom<proto::WireguardConfig> for wireguard::ConnectionConfig {
             exit_peer: None,
             ipv4_gateway,
             ipv6_gateway,
+            // NOTE: Not visible to protobuf clients, and custom tunnels cannot set this.
+            routes: None,
             #[cfg(target_os = "linux")]
             fwmark: Some(mullvad_types::TUNNEL_FWMARK),
         })
diff --git a/talpid-types/src/net/wireguard.rs b/talpid-types/src/net/wireguard.rs
index 5ef23b5100..53c593153d 100644
--- a/talpid-types/src/net/wireguard.rs
+++ b/talpid-types/src/net/wireguard.rs
@@ -72,6 +72,9 @@ pub struct ConnectionConfig {
     /// Gateway used by the tunnel (a private address).
     pub ipv4_gateway: Ipv4Addr,
     pub ipv6_gateway: Option<Ipv6Addr>,
+    /// Networks to route into the tunnel. If not set, this is the union of peers' allowed IPs.
+    #[serde(default)]
+    pub routes: Option<Vec<IpNetwork>>,
     #[cfg(target_os = "linux")]
     pub fwmark: Option<u32>,
 }
diff --git a/talpid-wireguard/src/config.rs b/talpid-wireguard/src/config.rs
index 30496c27ff..7a2f4cfaa0 100644
--- a/talpid-wireguard/src/config.rs
+++ b/talpid-wireguard/src/config.rs
@@ -1,3 +1,4 @@
+use ipnetwork::IpNetwork;
 use std::net::{Ipv4Addr, Ipv6Addr};
 use talpid_types::net::{GenericTunnelOptions, obfuscation::Obfuscators, wireguard};
 
@@ -35,6 +36,9 @@ pub struct Config {
     pub quantum_resistant: bool,
     /// Enable DAITA
     pub daita: bool,
+    /// Networks routed into the tunnel device. Typically matches the union of all peers' allowed
+    /// IPs.
+    pub routes: Vec<IpNetwork>,
 }
 
 /// Configuration errors
@@ -105,6 +109,7 @@ impl Config {
             obfuscation_mtu,
             quantum_resistant: wg_options.quantum_resistant,
             daita: wg_options.daita,
+            routes: Vec::new(),
         };
 
         for peer in config.peers_mut() {
@@ -115,6 +120,20 @@ impl Config {
             }
         }
 
+        let routes: Vec<IpNetwork> = match &connection.routes {
+            Some(routes) => routes
+                .iter()
+                .copied()
+                .filter(|route| route.is_ipv4() || generic_options.enable_ipv6)
+                .collect(),
+            None => config
+                .peers()
+                .flat_map(|peer| peer.allowed_ips.iter())
+                .copied()
+                .collect(),
+        };
+        config.routes = routes;
+
         Ok(config)
     }
 
@@ -164,11 +183,9 @@ impl Config {
             .chain(std::iter::once(&mut self.entry_peer))
     }
 
-    /// Return routes for all allowed IPs.
-    pub fn get_tunnel_destinations(&self) -> impl Iterator<Item = ipnetwork::IpNetwork> + '_ {
-        self.peers()
-            .flat_map(|peer| peer.allowed_ips.iter())
-            .cloned()
+    /// Return the networks routed into the tunnel device.
+    pub fn get_tunnel_destinations(&self) -> impl Iterator<Item = IpNetwork> + '_ {
+        self.routes.iter().copied()
     }
 }
 
@@ -176,7 +193,6 @@ impl Config {
 /// Used to block traffic to other destinations while connecting on Android.
 #[cfg(target_os = "android")]
 pub(crate) fn patch_allowed_ips(mut config: Config) -> Config {
-    use ipnetwork::IpNetwork;
     use std::net::IpAddr;
 
     let gateway_net_v4 = IpNetwork::from(IpAddr::from(config.ipv4_gateway));
diff --git a/talpid-wireguard/src/wireguard_nt/mod.rs b/talpid-wireguard/src/wireguard_nt/mod.rs
index ed23478bdd..f20e0013b9 100644
--- a/talpid-wireguard/src/wireguard_nt/mod.rs
+++ b/talpid-wireguard/src/wireguard_nt/mod.rs
@@ -1236,6 +1236,7 @@ mod tests {
         obfuscation_mtu: 0,
         quantum_resistant: false,
         daita: false,
+        routes: vec!["1.3.3.0/24".parse().unwrap()],
     });
 
     static WG_STRUCT_CONFIG: LazyLock<Interface> = LazyLock::new(|| Interface {
diff --git a/test/test-manager/src/tests/dns.rs b/test/test-manager/src/tests/dns.rs
index 2762aa543c..2bbb93293b 100644
--- a/test/test-manager/src/tests/dns.rs
+++ b/test/test-manager/src/tests/dns.rs
@@ -665,6 +665,7 @@ async fn connect_local_wg_relay(mullvad_client: &mut MullvadProxyClient) -> Resu
             },
             ipv4_gateway: CUSTOM_TUN_GATEWAY,
             exit_peer: None,
+            routes: None,
             #[cfg(target_os = "linux")]
             fwmark: None,
             ipv6_gateway: None,
diff --git a/test/test-manager/src/tests/helpers.rs b/test/test-manager/src/tests/helpers.rs
index 29255c8148..1261019db2 100644
--- a/test/test-manager/src/tests/helpers.rs
+++ b/test/test-manager/src/tests/helpers.rs
@@ -662,6 +662,7 @@ pub fn unreachable_wireguard_tunnel() -> talpid_types::net::wireguard::Connectio
         exit_peer: None,
         ipv4_gateway: Ipv4Addr::new(10, 64, 10, 1),
         ipv6_gateway: None,
+        routes: None,
         #[cfg(target_os = "linux")]
         fwmark: None,
     }