diff --git a/DEVELOPMENT.md b/DEVELOPMENT.md
index 21d73de00..68c99100e 100644
--- a/DEVELOPMENT.md
+++ b/DEVELOPMENT.md
@@ -39,6 +39,19 @@ source .venv/bin/activate
 ./foremanctl deploy --initial-admin-password=changeme --tuning development --initial-organization "Foreman CI" --initial-location "Internet"
 ```
 
+### Running Multiple Checkouts Simultaneously
+
+If you have multiple clones or git worktrees of this repo and want to run Vagrant VMs for each at the same time, set the `FOREMANCTL_VAGRANT_PREFIX` environment variable before starting VMs:
+
+```
+export FOREMANCTL_VAGRANT_PREFIX=1
+./forge vms start
+```
+
+When set, the Vagrantfile generates a unique 8-character prefix from an MD5 hash of the working directory path. This prefix is applied to both the libvirt domain names and VM hostnames, preventing collisions between deployments.
+
+Without the variable set, behavior is unchanged and VMs use the default hostnames.
+
 ### Deploy hammer (optional)
 
 ```
diff --git a/Vagrantfile b/Vagrantfile
index 99a51ae70..d2e2b3c56 100644
--- a/Vagrantfile
+++ b/Vagrantfile
@@ -1,4 +1,7 @@
+require 'digest'
+
 DOMAIN = ENV.fetch('VAGRANT_DOMAIN', 'example.com'.freeze)
+prefix = ENV.key?('FOREMANCTL_VAGRANT_PREFIX') ? Digest::MD5.hexdigest(Dir.pwd)[0..7] : nil
 
 Vagrant.configure("2") do |config|
   config.vm.synced_folder ".", "/vagrant"
@@ -18,9 +21,10 @@ Vagrant.configure("2") do |config|
 
   config.vm.define "quadlet" do |override|
     override.vm.box = ENV.fetch("FOREMANCTL_BASE_BOX", "centos/stream9")
-    override.vm.hostname = "quadlet.#{DOMAIN}"
+    override.vm.hostname = prefix ? "quadlet.#{prefix}.#{DOMAIN}" : "quadlet.#{DOMAIN}"
 
     override.vm.provider "libvirt" do |libvirt, provider|
+      libvirt.default_prefix = prefix if prefix
       libvirt.memory = 10240
       libvirt.cpus = 4
       libvirt.machine_virtual_size = 30
@@ -29,18 +33,20 @@ Vagrant.configure("2") do |config|
 
   config.vm.define "client" do |override|
     override.vm.box = "centos/stream9"
-    override.vm.hostname = "client.#{DOMAIN}"
+    override.vm.hostname = prefix ? "client.#{prefix}.#{DOMAIN}" : "client.#{DOMAIN}"
 
     override.vm.provider "libvirt" do |libvirt, provider|
+      libvirt.default_prefix = prefix if prefix
       libvirt.memory = 1024
     end
   end
 
   config.vm.define "database" do |override|
     override.vm.box = "centos/stream9"
-    override.vm.hostname = "database.#{DOMAIN}"
+    override.vm.hostname = prefix ? "database.#{prefix}.#{DOMAIN}" : "database.#{DOMAIN}"
 
     override.vm.provider "libvirt" do |libvirt, provider|
+      libvirt.default_prefix = prefix if prefix
       libvirt.memory = 2048
     end
   end
diff --git a/tests/conftest.py b/tests/conftest.py
index 9bf66ec3b..54551a352 100644
--- a/tests/conftest.py
+++ b/tests/conftest.py
@@ -63,7 +63,7 @@ def server_hostname():
 
 @pytest.fixture(scope="module")
 def server_fqdn(server):
-    return server.check_output('hostname -f')
+    return server.backend.hostname
 
 
 @pytest.fixture(scope="module")
@@ -73,7 +73,7 @@ def client_hostname():
 
 @pytest.fixture(scope="module")
 def client_fqdn(client):
-    return client.check_output('hostname -f')
+    return client.backend.hostname
 
 
 @pytest.fixture(scope="module")