diff --git a/releasenotes/notes/networkd_multiple_routes-becb9e691f38987a.yaml b/releasenotes/notes/networkd_multiple_routes-becb9e691f38987a.yaml
new file mode 100644
index 0000000..0cf26db
--- /dev/null
+++ b/releasenotes/notes/networkd_multiple_routes-becb9e691f38987a.yaml
@@ -0,0 +1,11 @@
+---
+
+fixes:
+  - |
+    Multiple routes can be supplied to the systemd network and they will be
+    placed to a separate configuration file
+    `/etc/systemd/network/{{ filename }}.d/routes.conf`
+
+    Previously defining multiple routes will result in squashing them together
+    under same section name, while for them to work properly each descriped
+    route must be placed in it's own section.
diff --git a/tasks/main.yml b/tasks/main.yml
index ecf6ab6..a109255 100644
--- a/tasks/main.yml
+++ b/tasks/main.yml
@@ -184,6 +184,24 @@
   tags:
     - systemd-networkd
 
+- name: Create systemd-networkd extra config folder
+  ansible.builtin.file:
+    path: "/etc/systemd/network/{{ item }}.network.d"
+    owner: "root"
+    group: "root"
+    mode: "0755"
+    state: directory
+  loop: "{{ _systemd_networks_named | selectattr('static_routes', 'defined') | map(attribute='filename') }}"
+
+- name: Place systemd-networkd network routes
+  ansible.builtin.template:
+    src: systemd-network-routes.j2
+    dest: "/etc/systemd/network/{{ item['filename'] }}.network.d/routes.conf"
+    owner: "root"
+    group: "root"
+    mode: "0644"
+  loop: "{{ _systemd_networks_named | selectattr('static_routes', 'defined') }}"
+
 - name: Enable and start systemd-networkd
   systemd:
     name: "systemd-networkd"
diff --git a/templates/systemd-network-routes.j2 b/templates/systemd-network-routes.j2
new file mode 100644
index 0000000..81f9e06
--- /dev/null
+++ b/templates/systemd-network-routes.j2
@@ -0,0 +1,9 @@
+# {{ ansible_managed }}
+
+{% for route in item['static_routes'] %}
+[Route]
+Destination={{ route['cidr'] }}
+Gateway={{ route['gateway'] }}
+Metric={{ 20 + loop.index }}
+
+{% endfor %}
diff --git a/templates/systemd-network.j2 b/templates/systemd-network.j2
index 8546043..75fca96 100644
--- a/templates/systemd-network.j2
+++ b/templates/systemd-network.j2
@@ -10,14 +10,6 @@ UseNTP=yes
 RouteMetric=20
 {% endif %}
 
-{% for route in item.1.static_routes | default([]) %}
-[Route]
-Destination={{ route['cidr'] }}
-Gateway={{ route['gateway'] }}
-Metric={{ 20 + loop.index }}
-
-{% endfor %}
-
 {%- if item.1.address is not defined %}
 {#   Address is not defined #}
 {%   set _addresses = [] %}