diff --git a/flake.nix b/flake.nix
index ef5b43f9c..ac4ef0d7c 100644
--- a/flake.nix
+++ b/flake.nix
@@ -161,6 +161,17 @@
       default = self.nixosModules.override;
     };
 
+    checks = eachSystem (pkgs: {
+      single = import ./nixos/tests/single.nix {
+        inherit self pkgs;
+        inherit (pkgs) lib;
+      };
+      multi = import ./nixos/tests/multi.nix {
+        inherit self pkgs;
+        inherit (pkgs) lib;
+      };
+    });
+
     devShells = eachSystem (pkgs: {
       default = pkgs.mkShell {
         packages = with pkgs; [
diff --git a/nixos/tests/multi.nix b/nixos/tests/multi.nix
new file mode 100644
index 000000000..3a250f2fb
--- /dev/null
+++ b/nixos/tests/multi.nix
@@ -0,0 +1,183 @@
+# Copyright (c) Tailscale Inc & AUTHORS
+# SPDX-License-Identifier: BSD-3-Clause
+#
+# NixOS VM test: multiple Tailscale instances on the same host
+# connecting to different Headscale coordination servers.
+# Verifies per-instance isolation (sockets, state dirs, service names),
+# CLI wrappers, and independent operation.
+{
+  self,
+  pkgs,
+  lib,
+}:
+pkgs.testers.runNixOSTest {
+  name = "tailscale-multi-instance";
+
+  nodes = let
+    mkCert = hostname:
+      pkgs.runCommand "selfSignedCerts-${hostname}" {
+        buildInputs = [pkgs.openssl];
+      } ''
+        openssl req -x509 -newkey rsa:4096 -sha256 -days 365 \
+          -nodes -out cert.pem -keyout key.pem \
+          -subj '/CN=${hostname}' \
+          -addext "subjectAltName=DNS:${hostname}"
+        mkdir -p $out
+        cp key.pem cert.pem $out
+      '';
+
+    cert1 = mkCert "headscale1";
+    cert2 = mkCert "headscale2";
+
+    headscalePort = 8080;
+    stunPort = 3478;
+
+    mkHeadscaleNode = {
+      hostname,
+      cert,
+      ipv4Prefix,
+    }: {
+      services.headscale = {
+        enable = true;
+        port = headscalePort;
+        settings = {
+          server_url = "https://${hostname}";
+          prefixes.v4 = ipv4Prefix;
+          derp.server = {
+            enabled = true;
+            region_id = 999;
+            stun_listen_addr = "0.0.0.0:${toString stunPort}";
+          };
+          dns = {
+            base_domain = "tailnet";
+            override_local_dns = false;
+          };
+        };
+      };
+
+      services.nginx = {
+        enable = true;
+        virtualHosts.${hostname} = {
+          addSSL = true;
+          sslCertificate = "${cert}/cert.pem";
+          sslCertificateKey = "${cert}/key.pem";
+          locations."/" = {
+            proxyPass = "http://127.0.0.1:${toString headscalePort}";
+            proxyWebsockets = true;
+          };
+        };
+      };
+
+      networking.firewall = {
+        allowedTCPPorts = [80 443];
+        allowedUDPPorts = [stunPort];
+      };
+      environment.systemPackages = [pkgs.headscale];
+    };
+  in {
+    headscale1 = mkHeadscaleNode {
+      hostname = "headscale1";
+      cert = cert1;
+      ipv4Prefix = "100.64.0.0/24";
+    };
+    headscale2 = mkHeadscaleNode {
+      hostname = "headscale2";
+      cert = cert2;
+      ipv4Prefix = "100.64.1.0/24";
+    };
+
+    # Client running two Tailscale instances (userspace mode by default)
+    client = {
+      imports = [self.nixosModules.override];
+      services.tailscales = {
+        net1.enable = true;
+        net2.enable = true;
+      };
+      security.pki.certificateFiles = [
+        "${cert1}/cert.pem"
+        "${cert2}/cert.pem"
+      ];
+    };
+
+    # A peer on headscale1's network (TUN mode, single instance)
+    peer1 = {
+      imports = [self.nixosModules.override];
+      services.tailscale = {
+        enable = true;
+        openFirewall = true;
+      };
+      security.pki.certificateFiles = ["${cert1}/cert.pem"];
+    };
+  };
+
+  testScript = ''
+    start_all()
+
+    # Wait for both headscale servers
+    headscale1.wait_for_unit("headscale")
+    headscale1.wait_for_open_port(443)
+    headscale2.wait_for_unit("headscale")
+    headscale2.wait_for_open_port(443)
+
+    # Wait for client's tailscaled instances
+    client.wait_for_unit("tailscaled-net1.service")
+    client.wait_for_unit("tailscaled-net2.service")
+
+    # Wait for peer1's tailscaled
+    peer1.wait_for_unit("tailscaled.service")
+
+    # Create users and auth keys on both headscale servers.
+    # headscale CLI uses numeric user IDs: first user gets ID 1.
+    headscale1.succeed("headscale users create user1")
+    authkey1 = headscale1.succeed(
+        "headscale preauthkeys create -u 1 --reusable"
+    ).strip()
+
+    headscale2.succeed("headscale users create user2")
+    authkey2 = headscale2.succeed(
+        "headscale preauthkeys create -u 1 --reusable"
+    ).strip()
+
+    # Join client's instances to their respective headscale servers.
+    # Use succeed() to ensure the commands don't fail silently.
+    client.succeed(
+        f"tailscale-net1 up --login-server 'https://headscale1' --auth-key {authkey1}"
+    )
+    client.succeed(
+        f"tailscale-net2 up --login-server 'https://headscale2' --auth-key {authkey2}"
+    )
+
+    # Join peer1 to headscale1
+    peer1.succeed(
+        f"tailscale up --login-server 'https://headscale1' --auth-key {authkey1}"
+    )
+
+    # Verify both instances are connected
+    client.wait_until_succeeds("tailscale-net1 status", timeout=60)
+    client.wait_until_succeeds("tailscale-net2 status", timeout=60)
+
+    # Verify socket isolation
+    client.succeed("test -S /run/tailscale-net1/tailscaled.sock")
+    client.succeed("test -S /run/tailscale-net2/tailscaled.sock")
+
+    # Verify state directory isolation
+    client.succeed("test -d /var/lib/tailscale-net1")
+    client.succeed("test -d /var/lib/tailscale-net2")
+
+    # Get tailscale IPs from both instances
+    ip_net1 = client.succeed("tailscale-net1 ip -4").strip()
+    ip_net2 = client.succeed("tailscale-net2 ip -4").strip()
+
+    # Verify the IPs are different (different tailnets)
+    assert ip_net1 != ip_net2, f"Expected different IPs, got {ip_net1} for both"
+
+    # Verify net1 can reach peer1 via tailscale ping
+    client.wait_until_succeeds("tailscale-net1 ping peer1", timeout=60)
+
+    # Test that restarting one instance doesn't affect the other
+    client.succeed("systemctl restart tailscaled-net1")
+    client.wait_for_unit("tailscaled-net1.service")
+    client.succeed("tailscale-net2 status")
+    client.wait_until_succeeds("tailscale-net1 status", timeout=30)
+  '';
+}
diff --git a/nixos/tests/single.nix b/nixos/tests/single.nix
new file mode 100644
index 000000000..2cd765fb6
--- /dev/null
+++ b/nixos/tests/single.nix
@@ -0,0 +1,120 @@
+# Copyright (c) Tailscale Inc & AUTHORS
+# SPDX-License-Identifier: BSD-3-Clause
+#
+# NixOS VM test: single Tailscale instance connecting to Headscale.
+# Verifies the basic module functionality, peer-to-peer connectivity,
+# and service restart resilience.
+{
+  self,
+  pkgs,
+  lib,
+}:
+pkgs.testers.runNixOSTest {
+  name = "tailscale-single-instance";
+
+  nodes = let
+    tls-cert = pkgs.runCommand "selfSignedCerts" {
+      buildInputs = [pkgs.openssl];
+    } ''
+      openssl req -x509 -newkey rsa:4096 -sha256 -days 365 \
+        -nodes -out cert.pem -keyout key.pem \
+        -subj '/CN=headscale' -addext "subjectAltName=DNS:headscale"
+      mkdir -p $out
+      cp key.pem cert.pem $out
+    '';
+
+    headscalePort = 8080;
+    stunPort = 3478;
+
+    peerConfig = {
+      imports = [self.nixosModules.override];
+      services.tailscale = {
+        enable = true;
+        openFirewall = true;
+      };
+      security.pki.certificateFiles = ["${tls-cert}/cert.pem"];
+    };
+  in {
+    peer1 = peerConfig;
+    peer2 = peerConfig;
+
+    headscale = {
+      services.headscale = {
+        enable = true;
+        port = headscalePort;
+        settings = {
+          server_url = "https://headscale";
+          prefixes.v4 = "100.64.0.0/10";
+          derp.server = {
+            enabled = true;
+            region_id = 999;
+            stun_listen_addr = "0.0.0.0:${toString stunPort}";
+          };
+          dns = {
+            base_domain = "tailnet";
+            override_local_dns = false;
+          };
+        };
+      };
+
+      services.nginx = {
+        enable = true;
+        virtualHosts.headscale = {
+          addSSL = true;
+          sslCertificate = "${tls-cert}/cert.pem";
+          sslCertificateKey = "${tls-cert}/key.pem";
+          locations."/" = {
+            proxyPass = "http://127.0.0.1:${toString headscalePort}";
+            proxyWebsockets = true;
+          };
+        };
+      };
+
+      networking.firewall = {
+        allowedTCPPorts = [80 443];
+        allowedUDPPorts = [stunPort];
+      };
+      environment.systemPackages = [pkgs.headscale];
+    };
+  };
+
+  testScript = ''
+    start_all()
+
+    # Wait for headscale
+    headscale.wait_for_unit("headscale")
+    headscale.wait_for_open_port(443)
+
+    # Verify our tailscaled service starts on peers
+    peer1.wait_for_unit("tailscaled.service")
+    peer2.wait_for_unit("tailscaled.service")
+
+    # Create user and auth key.
+    # headscale CLI uses numeric user IDs: first user gets ID 1.
+    headscale.succeed("headscale users create testuser")
+    authkey = headscale.succeed(
+        "headscale preauthkeys create -u 1 --reusable"
+    ).strip()
+
+    # Join peers to tailnet
+    peer1.execute(
+        f"tailscale up --login-server 'https://headscale' --auth-key {authkey}"
+    )
+    peer2.execute(
+        f"tailscale up --login-server 'https://headscale' --auth-key {authkey}"
+    )
+
+    # Verify peer-to-peer connectivity
+    peer1.wait_until_succeeds("tailscale ping peer2", timeout=60)
+    peer2.wait_until_succeeds("tailscale ping peer1", timeout=60)
+
+    # Verify tailscale status
+    peer1.succeed("tailscale status")
+    peer2.succeed("tailscale status")
+
+    # Test service restart resilience
+    peer1.succeed("systemctl restart tailscaled")
+    peer1.wait_for_unit("tailscaled.service")
+    peer1.wait_until_succeeds("tailscale ping peer2", timeout=60)
+  '';
+}