diff --git a/flake.nix b/flake.nix
index fc8daf201..9772fa07b 100644
--- a/flake.nix
+++ b/flake.nix
@@ -47,6 +47,11 @@
         system: let
           pkgs-stable = nixpkgs-stable.legacyPackages.${system};
           pkgs-unstable = nixpkgs-unstable.legacyPackages.${system};
+
+          # These are all of our VM tests.
+          tests = import ./nix/tests/default.nix {
+            nixpkgs = pkgs-unstable;
+          };
         in {
           devShell.${system} = pkgs-stable.callPackage ./nix/devShell.nix {
             zig = zig.packages.${system}."0.14.0";
@@ -72,6 +77,8 @@
 
           formatter.${system} = pkgs-stable.alejandra;
 
+          checks.${system} = tests;
+
           apps.${system} = let
             runVM = (
               module: let
@@ -91,15 +98,29 @@
                 program = "${program}";
               }
             );
-          in {
-            wayland-cinnamon = runVM ./nix/vm/wayland-cinnamon.nix;
-            wayland-gnome = runVM ./nix/vm/wayland-gnome.nix;
-            wayland-plasma6 = runVM ./nix/vm/wayland-plasma6.nix;
-            x11-cinnamon = runVM ./nix/vm/x11-cinnamon.nix;
-            x11-gnome = runVM ./nix/vm/x11-gnome.nix;
-            x11-plasma6 = runVM ./nix/vm/x11-plasma6.nix;
-            x11-xfce = runVM ./nix/vm/x11-xfce.nix;
-          };
+          in
+            {
+              wayland-cinnamon = runVM ./nix/vm/wayland-cinnamon.nix;
+              wayland-gnome = runVM ./nix/vm/wayland-gnome.nix;
+              wayland-plasma6 = runVM ./nix/vm/wayland-plasma6.nix;
+              x11-cinnamon = runVM ./nix/vm/x11-cinnamon.nix;
+              x11-gnome = runVM ./nix/vm/x11-gnome.nix;
+              x11-plasma6 = runVM ./nix/vm/x11-plasma6.nix;
+              x11-xfce = runVM ./nix/vm/x11-xfce.nix;
+            }
+            // (pkgs-stable.lib.mapAttrs' (
+                # This adds all of our VM tests as runnable apps that load
+                # the interactive driver (repl). We map all the names of the
+                # tests to "test-<name>" so its distinct from other apps.
+                name: value: {
+                  name = "test-${name}";
+                  value = {
+                    type = "app";
+                    program = pkgs-unstable.lib.getExe tests.${name}.driverInteractive;
+                  };
+                }
+              )
+              tests);
         }
         # Our supported systems are the same supported systems as the Zig binaries.
       ) (builtins.attrNames zig.packages)
diff --git a/nix/tests/basic.nix b/nix/tests/basic.nix
new file mode 100644
index 000000000..4822c1500
--- /dev/null
+++ b/nix/tests/basic.nix
@@ -0,0 +1,26 @@
+{
+  name = "basic";
+
+  nodes.machine = {
+    config,
+    pkgs,
+    ...
+  }: {
+    users.users.alice = {
+      isNormalUser = true;
+      extraGroups = ["wheel"];
+      packages = with pkgs; [
+        firefox
+        (pkgs.callPackage ../package.nix {})
+      ];
+    };
+
+    system.stateVersion = "24.11";
+  };
+
+  testScript = ''
+    machine.wait_for_unit("default.target")
+    machine.succeed("su -- alice -c 'which firefox'")
+    machine.fail("su -- root -c 'which firefox'")
+  '';
+}
diff --git a/nix/tests/default.nix b/nix/tests/default.nix
new file mode 100644
index 000000000..6abab82ce
--- /dev/null
+++ b/nix/tests/default.nix
@@ -0,0 +1,14 @@
+{nixpkgs}: let
+  # mkTest does nothing special right now, its just a wrapper around
+  # runNixOSTest, but it could be extended in the future so I pulled it out.
+  mkTest = path:
+    nixpkgs.testers.runNixOSTest {
+      imports = [
+        path
+      ];
+    };
+in {
+  basic = mkTest ./basic.nix;
+  gnome = mkTest ./gnome.nix;
+  i3 = mkTest ./i3.nix;
+}
diff --git a/nix/tests/gnome.nix b/nix/tests/gnome.nix
new file mode 100644
index 000000000..dd0176596
--- /dev/null
+++ b/nix/tests/gnome.nix
@@ -0,0 +1,56 @@
+{
+  name = "gnome";
+
+  nodes.machine = {
+    config,
+    pkgs,
+    ...
+  }: {
+    users.users.alice = {
+      isNormalUser = true;
+      password = "alice";
+      extraGroups = ["wheel"];
+      packages = with pkgs; [
+        (pkgs.callPackage ../package.nix {})
+      ];
+    };
+
+    services.xserver.enable = true;
+
+    services.xserver.displayManager = {
+      gdm.enable = true;
+      gdm.debug = true;
+    };
+
+    services.displayManager.autoLogin = {
+      enable = true;
+      user = "alice";
+    };
+
+    services.xserver.desktopManager.gnome.enable = true;
+    services.xserver.desktopManager.gnome.debug = true;
+
+    systemd.user.services = {
+      "org.gnome.Shell@wayland" = {
+        serviceConfig = {
+          ExecStart = [
+            # Clear the list before overriding it.
+            ""
+            # Eval API is now internal so Shell needs to run in unsafe mode.
+            # TODO: improve test driver so that it supports openqa-like manipulation
+            # that would allow us to drop this mess.
+            "${pkgs.gnome-shell}/bin/gnome-shell --unsafe-mode"
+          ];
+        };
+      };
+    };
+
+    system.stateVersion = "24.11";
+  };
+
+  testScript = ''
+    machine.wait_for_unit("default.target")
+    machine.succeed("su -- alice -c 'which firefox'")
+    machine.fail("su -- root -c 'which firefox'")
+  '';
+}
diff --git a/nix/tests/i3.nix b/nix/tests/i3.nix
new file mode 100644
index 000000000..c1d5811f6
--- /dev/null
+++ b/nix/tests/i3.nix
@@ -0,0 +1,59 @@
+{
+  name = "gnome";
+
+  nodes.machine = {
+    config,
+    pkgs,
+    ...
+  }: {
+    users.users.alice = {
+      isNormalUser = true;
+      password = "alice";
+      extraGroups = ["wheel"];
+      packages = with pkgs; [
+        (pkgs.callPackage ../package.nix {})
+      ];
+    };
+
+    # We need an XDG portal for various applications to work properly,
+    # such as Flatpak applications.
+    xdg.portal = {
+      enable = true;
+      extraPortals = [ pkgs.xdg-desktop-portal-gtk ];
+      config.common.default = "*";
+    };
+
+    services.xserver = {
+      enable = true;
+      xkb.layout = "us";
+      dpi = 220;
+
+      desktopManager = {
+        xterm.enable = false;
+        wallpaper.mode = "fill";
+      };
+
+      displayManager = {
+        defaultSession = "none+i3";
+        lightdm.enable = true;
+      };
+
+      windowManager = {
+        i3.enable = true;
+      };
+    };
+
+    services.displayManager.autoLogin = {
+      enable = true;
+      user = "alice";
+    };
+
+    system.stateVersion = "24.11";
+  };
+
+  testScript = ''
+    machine.wait_for_unit("default.target")
+    machine.succeed("su -- alice -c 'which firefox'")
+    machine.fail("su -- root -c 'which firefox'")
+  '';
+}