diff --git a/changelogs/fragments/ansible-test-inventory-json.yml b/changelogs/fragments/ansible-test-inventory-json.yml
new file mode 100644
index 00000000000..98bff49de6d
--- /dev/null
+++ b/changelogs/fragments/ansible-test-inventory-json.yml
@@ -0,0 +1,4 @@
+minor_changes:
+  - >-
+    ansible-test - add ``.winrm`` and ``.networking`` as valid JSON/YAML inventory file extensions. This should not
+    affect any public facing code as it is used internally for inventories generated by ``ansible-test``.
diff --git a/test/lib/ansible_test/_internal/ansible_util.py b/test/lib/ansible_test/_internal/ansible_util.py
index 1c42ccae951..16eb8bdf8de 100644
--- a/test/lib/ansible_test/_internal/ansible_util.py
+++ b/test/lib/ansible_test/_internal/ansible_util.py
@@ -93,6 +93,7 @@ def ansible_environment(args: CommonConfig, color: bool = True, ansible_config:
 
     ansible = dict(
         ANSIBLE_PYTHON_MODULE_RLIMIT_NOFILE=str(SOFT_RLIMIT_NOFILE),
+        ANSIBLE_INVENTORY_PLUGIN_EXTS='.yaml, .yml, .json, .winrm, .networking',  # allows the yaml/json inventory format for windows and networking
         ANSIBLE_FORCE_COLOR='%s' % 'true' if args.color and color else 'false',
         ANSIBLE_FORCE_HANDLERS='true',  # allow cleanup handlers to run when tests fail
         ANSIBLE_HOST_PATTERN_MISMATCH='error',  # prevent tests from unintentionally passing when hosts are not found
diff --git a/test/lib/ansible_test/_internal/host_profiles.py b/test/lib/ansible_test/_internal/host_profiles.py
index c72733f814a..fcfb88f5eb9 100644
--- a/test/lib/ansible_test/_internal/host_profiles.py
+++ b/test/lib/ansible_test/_internal/host_profiles.py
@@ -202,31 +202,24 @@ class Inventory:
     def write(self, args: CommonConfig, path: str) -> None:
         """Write the given inventory to the specified path on disk."""
 
-        # NOTE: Switching the inventory generation to write JSON would be nice, but is currently not possible due to the use of hard-coded inventory filenames.
-        #       The name `inventory` works for the POSIX integration tests, but `inventory.winrm` and `inventory.networking` will only parse in INI format.
-        #       If tests are updated to use the `INVENTORY_PATH` environment variable, then this could be changed.
-        #       Also, some tests detect the test type by inspecting the suffix on the inventory filename, which would break if it were changed.
-
-        inventory_text = ''
+        inventory_data: dict[str, dict[str, dict[str, dict[str, object]]]] = dict()
 
         for group, hosts in self.host_groups.items():
-            inventory_text += f'[{group}]\n'
+            group_data = inventory_data.setdefault(group, dict())
+            hosts_data = group_data.setdefault('hosts', dict())
 
             for host, variables in hosts.items():
-                kvp = ' '.join(f"{key}={value!r}" for key, value in variables.items())
-                inventory_text += f'{host} {kvp}\n'
-
-            inventory_text += '\n'
+                host_entry = hosts_data.setdefault(host, dict())
+                host_entry.update(variables)
 
         for group, children in (self.extra_groups or {}).items():
-            inventory_text += f'[{group}]\n'
+            group_data = inventory_data.setdefault(group, dict())
+            group_children = group_data.setdefault('children', dict())
 
             for child in children:
-                inventory_text += f'{child}\n'
-
-            inventory_text += '\n'
+                group_children[child] = dict()
 
-        inventory_text = inventory_text.strip()
+        inventory_text = json.dumps(inventory_data, indent=4)
 
         if not args.explain:
             write_text_file(path, inventory_text + '\n')
@@ -1380,7 +1373,7 @@ class NetworkRemoteProfile(RemoteProfile[NetworkRemoteConfig]):
         env = ansible_environment(self.args)
         module_name = f'{self.config.collection + "." if self.config.collection else ""}{self.config.platform}_command'
 
-        with tempfile.NamedTemporaryFile() as inventory_file:
+        with tempfile.NamedTemporaryFile(suffix='.json') as inventory_file:
             inventory.write(self.args, inventory_file.name)
 
             cmd = ['ansible', '-m', module_name, '-a', 'commands=?', '-i', inventory_file.name, 'all']
@@ -1636,7 +1629,7 @@ class WindowsRemoteProfile(RemoteProfile[WindowsRemoteConfig]):
         env = ansible_environment(self.args)
         module_name = 'ansible.windows.win_ping'
 
-        with tempfile.NamedTemporaryFile() as inventory_file:
+        with tempfile.NamedTemporaryFile(suffix='.json') as inventory_file:
             inventory.write(self.args, inventory_file.name)
 
             cmd = ['ansible', '-m', module_name, '-i', inventory_file.name, 'all']
diff --git a/test/lib/ansible_test/_internal/inventory.py b/test/lib/ansible_test/_internal/inventory.py
index 26f8f8bd650..4aa2fd008f1 100644
--- a/test/lib/ansible_test/_internal/inventory.py
+++ b/test/lib/ansible_test/_internal/inventory.py
@@ -109,9 +109,7 @@ def create_windows_inventory(args: EnvironmentConfig, path: str, target_hosts: l
         # The `testhost` group is needed to support the `binary_modules_winrm` integration test.
         # The test should be updated to remove the need for this.
         extra_groups={
-            'testhost:children': [
-                'windows',
-            ],
+            'testhost': ['windows'],
         },
     )
 
@@ -145,7 +143,7 @@ def create_network_inventory(args: EnvironmentConfig, path: str, target_hosts: l
         # see: https://github.com/ansible/ansible/pull/34661
         # see: https://github.com/ansible/ansible/pull/34707
         extra_groups={
-            'net:children': sorted(host_groups),
+            'net': list(sorted(host_groups)),
         },
     )