diff --git a/conf/dynaconf_hooks.py b/conf/dynaconf_hooks.py
index 03807f5a211..8f7249b4aac 100644
--- a/conf/dynaconf_hooks.py
+++ b/conf/dynaconf_hooks.py
@@ -30,7 +30,7 @@ def post(settings):
             )
             data = get_repos_config(settings)
             write_cache(settings_cache_path, data)
-    ipv6_hostname_translation(settings, data)
+    ipv6_hostname_translation(settings)
     config_migrations(settings, data)
     data['dynaconf_merge'] = True
     return data
diff --git a/robottelo/config/__init__.py b/robottelo/config/__init__.py
index 13769cdef2a..10a7d54e0f5 100644
--- a/robottelo/config/__init__.py
+++ b/robottelo/config/__init__.py
@@ -16,6 +16,32 @@
     os.environ['ROBOTTELO_DIR'] = str(robottelo_root_dir)
 
 
+# Define the function to replace 'ipv4' with 'ipv6' in URLs
+def replace_ipv4_with_ipv6_in_urls(settings):
+    def replace_in_value(value):
+        # Only replace 'ipv4' with 'ipv6' in strings that contain 'redhat.com'
+        if isinstance(value, str) and 'ipv4' in value and 'redhat.com' in value:
+            return value.replace('ipv4', 'ipv6')
+        return value
+
+    def resolve_and_replace(settings_dict):
+        resolved = {}
+        for key, value in settings_dict.items():
+            if isinstance(value, str):
+                resolved[key] = replace_in_value(value)
+            elif isinstance(value, dict):
+                # Recursively handle nested dictionaries
+                resolved[key] = resolve_and_replace(value)
+            else:
+                resolved[key] = value
+        return resolved
+
+    # Update the settings in-place with resolved and replaced values
+    updated_settings = resolve_and_replace(settings.as_dict())
+    for key, value in updated_settings.items():
+        settings.set(key, value)
+
+
 def get_settings():
     """Return Lazy settings object after validating
 
@@ -49,6 +75,8 @@ def get_settings():
 
 
 settings = get_settings()
+if settings.server.is_ipv6:
+    replace_ipv4_with_ipv6_in_urls(settings)
 robottelo_tmp_dir = Path(settings.robottelo.tmp_dir)
 robottelo_tmp_dir.mkdir(parents=True, exist_ok=True)
 
diff --git a/robottelo/utils/url.py b/robottelo/utils/url.py
index b60fc089e6e..df692dfd53d 100644
--- a/robottelo/utils/url.py
+++ b/robottelo/utils/url.py
@@ -16,36 +16,36 @@ def is_ipv4_url(text):
     return isinstance(text, str) and 'ipv4' in text and 'redhat.com' in text
 
 
-def ipv6_translator(settings_list, setting_major, data):
+def ipv6_translator(settings):
     """Translates the hostname containing IPv4 to IPv6 and updates the settings object"""
-    setting_major = list(map(str, setting_major))
-    dotted_settings = '.'.join(setting_major)
-    for _key, _val in settings_list.items():
-        if is_ipv4_url(_val):
-            data[f'{dotted_settings}.{_key}'] = str(_val).replace('ipv4', 'ipv6')
-            logger.debug(f'Setting translated to IPv6, Path: {dotted_settings}.{_key}')
-        elif isinstance(_val, list):
-            updated = False
-            new_list = _val
-            for i in range(len(new_list)):
-                if is_ipv4_url(new_list[i]):
-                    new_list[i] = new_list[i].replace('ipv4', 'ipv6')
-                    updated = True
-            if updated:
-                data[f'{dotted_settings}.{_key}'] = new_list
-                logger.debug(f'Setting translated to IPv6, Path: {dotted_settings}.{_key}')
-        elif isinstance(_val, dict):
-            new_setting_major = setting_major + [_key]
-            ipv6_translator(settings_list=_val, setting_major=new_setting_major, data=data)
-
-
-def ipv6_hostname_translation(settings, data):
+
+    def replace_in_value(value):
+        # Only replace 'ipv4' with 'ipv6' in strings that contain 'redhat.com'
+        if isinstance(value, str) and 'ipv4' in value and 'redhat.com' in value:
+            return value.replace('ipv4', 'ipv6')
+        return value
+
+    def resolve_and_replace(settings_dict):
+        resolved = {}
+        for key, value in settings_dict.items():
+            if isinstance(value, str):
+                resolved[key] = replace_in_value(value)
+            elif isinstance(value, dict):
+                # Recursively handle nested dictionaries
+                resolved[key] = resolve_and_replace(value)
+            else:
+                resolved[key] = value
+        return resolved
+
+    # Update the settings in-place with resolved and replaced values
+    updated_settings = resolve_and_replace(settings.as_dict())
+    for key, value in updated_settings.items():
+        settings.set(key, value)
+
+
+def ipv6_hostname_translation(settings):
     """Migrates any IPv4 containing hostname in conf to IPv6 hostname"""
-    settings_path = []
     if settings.server.is_ipv6:
-        all_settings = settings.loaded_by_loaders.items()
-        for loader_name, loader_settings in tuple(all_settings):
-            if loader_name.loader == 'yaml':
-                ipv6_translator(loader_settings, settings_path, data)
+        ipv6_translator(settings)
     else:
         logger.debug('IPv6 Hostname dynaconf migration hook is skipped for IPv4 testing')