diff --git a/Code/Framework/AzCore/AzCore/Component/ComponentApplication.cpp b/Code/Framework/AzCore/AzCore/Component/ComponentApplication.cpp
index b8d3e12712..5266cefca2 100644
--- a/Code/Framework/AzCore/AzCore/Component/ComponentApplication.cpp
+++ b/Code/Framework/AzCore/AzCore/Component/ComponentApplication.cpp
@@ -909,6 +909,8 @@ namespace AZ
         SettingsRegistryMergeUtils::MergeSettingsToRegistry_ProjectUserRegistry(registry, AZ_TRAIT_OS_PLATFORM_CODENAME, specializations, &scratchBuffer);
         SettingsRegistryMergeUtils::MergeSettingsToRegistry_CommandLine(registry, m_commandLine, true);
 #endif
+        // Update the Runtime file paths in case the "{BootstrapSettingsRootKey}/assets" key was overriden by a setting registry
+        AZ::SettingsRegistryMergeUtils::MergeSettingsToRegistry_AddRuntimeFilePaths(registry);
     }
 
     void ComponentApplication::SetSettingsRegistrySpecializations(SettingsRegistryInterface::Specializations& specializations)
diff --git a/Code/Framework/AzGameFramework/AzGameFramework/Application/GameApplication.cpp b/Code/Framework/AzGameFramework/AzGameFramework/Application/GameApplication.cpp
index f4fc9364f7..edd4af293d 100644
--- a/Code/Framework/AzGameFramework/AzGameFramework/Application/GameApplication.cpp
+++ b/Code/Framework/AzGameFramework/AzGameFramework/Application/GameApplication.cpp
@@ -80,6 +80,8 @@ namespace AzGameFramework
         AZ::SettingsRegistryMergeUtils::MergeSettingsToRegistry_ProjectUserRegistry(registry, AZ_TRAIT_OS_PLATFORM_CODENAME, specializations, &scratchBuffer);
         AZ::SettingsRegistryMergeUtils::MergeSettingsToRegistry_CommandLine(registry, m_commandLine, true);
 #endif
+        // Update the Runtime file paths in case the "{BootstrapSettingsRootKey}/assets" key was overriden by a setting registry
+        AZ::SettingsRegistryMergeUtils::MergeSettingsToRegistry_AddRuntimeFilePaths(registry);
     }
 
     AZ::ComponentTypeList GameApplication::GetRequiredSystemComponents() const