diff --git a/test/jslib/test_jslib_custom_settings.js b/test/jslib/test_jslib_custom_settings.js
index 2423a0574fc2d..3fa209787be3c 100644
--- a/test/jslib/test_jslib_custom_settings.js
+++ b/test/jslib/test_jslib_custom_settings.js
@@ -1,9 +1,5 @@
 addToLibrary({
-	js_function: function() {
-#if CUSTOM_JS_OPTION
-		return 1;
-#else
-		return 0;
-#endif
-	}
-});
+  js_function: function() {
+    return {{{ CUSTOM_JS_OPTION }}};
+  }
+});
\ No newline at end of file
diff --git a/test/test_jslib.py b/test/test_jslib.py
index 0c46710abc217..211a679386bd4 100644
--- a/test/test_jslib.py
+++ b/test/test_jslib.py
@@ -353,10 +353,15 @@ def test_jslib_legacy(self):
   # the -jsDfoo=val syntax:
   # See https://github.com/emscripten-core/emscripten/issues/10580.
   def test_jslib_custom_settings(self):
-    self.cflags += ['--js-library', test_file('jslib/test_jslib_custom_settings.js'), '-jsDCUSTOM_JS_OPTION=1']
-    self.do_run_in_out_file_test('jslib/test_jslib_custom_settings.c')
+    test_file_path = test_file('jslib/test_jslib_custom_settings.c')
+    js_lib = test_file('jslib/test_jslib_custom_settings.js')
 
-    self.assert_fail([EMCC, '-jsDWASM=0'], 'cannot change built-in settings values with a -jsD directive')
+    self.do_runf(test_file_path, '1\n', cflags=['--js-library', js_lib, '-jsDCUSTOM_JS_OPTION=1'])
+
+    # verify that the settings can be specified more than once, and that the last one wins.
+    self.do_runf(test_file_path, '2\n', cflags=['--js-library', js_lib, '-jsDCUSTOM_JS_OPTION=1', '-jsDCUSTOM_JS_OPTION=2'])
+
+    self.assert_fail([EMCC, '-jsDWASM=1'], 'cannot change built-in settings values with a -jsD directive')
 
   def test_jslib_native_deps(self):
     # Verify that memset (which lives in compiled code), can be specified as a JS library
diff --git a/tools/cmdline.py b/tools/cmdline.py
index d708a09f5c5a7..6584ea02e25a2 100644
--- a/tools/cmdline.py
+++ b/tools/cmdline.py
@@ -216,6 +216,7 @@ def parse_args(newargs):  # noqa: C901, PLR0912, PLR0915
   """
   should_exit = False
   skip = False
+  builtin_settings = set(settings.keys())
   LEGACY_ARGS = {'--js-opts', '--llvm-opts', '--llvm-lto', '--memory-init-file'}
   LEGACY_FLAGS = {'--separate-asm', '--jcache', '--proxy-to-worker', '--default-obj-ext',
                   '--embind-emit-tsd', '--remove-duplicates', '--no-heap-copy'}
@@ -572,12 +573,12 @@ def consume_arg_file():
     elif arg.startswith('-jsD'):
       key = arg.removeprefix('-jsD')
       if '=' in key:
-        key, value = key.split('=')
+        key, value = key.split('=', 1)
       else:
         value = '1'
-      if key in settings.keys():
+      if key in builtin_settings:
         exit_with_error(f'{arg}: cannot change built-in settings values with a -jsD directive. Pass -s{key}={value} instead!')
-      # Apply user -jsD settings
+      # Allow overrides/duplicates for user-defined -jsD flags
       settings[key] = value
       newargs[i] = ''
     elif check_flag('-shared'):