diff --git a/grr/client_builder/grr_response_client_builder/client_build.py b/grr/client_builder/grr_response_client_builder/client_build.py
index 7220d6ed0..323e866cc 100644
--- a/grr/client_builder/grr_response_client_builder/client_build.py
+++ b/grr/client_builder/grr_response_client_builder/client_build.py
@@ -423,9 +423,22 @@ def main(args):
 
   if args.subparser_name == "build":
     if grr_config.CONFIG.ContextApplied("Platform:Darwin"):
-      if not grr_config.CONFIG.Get("ClientBuilder.install_dir"):
+      # We know that the client builder is run on Darwin, so we can check that
+      # the required config options are set. But the builder config options use
+      # the "Target:Darwin" context, as they care about the target system that
+      # the template is built for, not the system that the builder is run on.
+      # The fact that we build macOS templates on Darwin is technically
+      # an implementation detail even though it is impossible to build macOS
+      # templates on any other platform.
+      if not grr_config.CONFIG.Get(
+          "ClientBuilder.install_dir",
+          context=[contexts.TARGET_DARWIN],
+      ):
         raise RuntimeError("ClientBuilder.install_dir must be set.")
-      if not grr_config.CONFIG.Get("ClientBuilder.fleetspeak_plist_path"):
+      if not grr_config.CONFIG.Get(
+          "ClientBuilder.fleetspeak_plist_path",
+          context=[contexts.TARGET_DARWIN],
+      ):
         raise RuntimeError("ClientBuilder.fleetspeak_plist_path must be set.")
     TemplateBuilder().BuildTemplate(context=context, output=args.output)
   elif args.subparser_name == "repack":