diff --git a/bundle-uri.c b/bundle-uri.c
index c02e7f62eb1..3d44ec2b1e6 100644
--- a/bundle-uri.c
+++ b/bundle-uri.c
@@ -173,6 +173,33 @@ static int bundle_list_update(const char *key, const char *value,
 	return 0;
 }
 
+static int config_to_bundle_list(const char *key, const char *value, void *data)
+{
+	struct bundle_list *list = data;
+	return bundle_list_update(key, value, list);
+}
+
+int bundle_uri_parse_config_format(const char *uri,
+				   const char *filename,
+				   struct bundle_list *list)
+{
+	int result;
+	struct config_options opts = {
+		.error_action = CONFIG_ERROR_ERROR,
+	};
+
+	result = git_config_from_file_with_options(config_to_bundle_list,
+						   filename, list,
+						   &opts);
+
+	if (!result && list->mode == BUNDLE_MODE_NONE) {
+		warning(_("bundle list at '%s' has no mode"), uri);
+		result = 1;
+	}
+
+	return result;
+}
+
 static char *find_temp_filename(void)
 {
 	int fd;
diff --git a/bundle-uri.h b/bundle-uri.h
index 0e56ab2ae5a..bc13d4c9929 100644
--- a/bundle-uri.h
+++ b/bundle-uri.h
@@ -62,6 +62,15 @@ int for_all_bundles_in_list(struct bundle_list *list,
 struct FILE;
 void print_bundle_list(FILE *fp, struct bundle_list *list);
 
+/**
+ * A bundle URI may point to a bundle list where the key=value
+ * pairs are provided in config file format. This method is
+ * exposed publicly for testing purposes.
+ */
+int bundle_uri_parse_config_format(const char *uri,
+				   const char *filename,
+				   struct bundle_list *list);
+
 /**
  * Fetch data from the given 'uri' and unbundle the bundle data found
  * based on that information.
diff --git a/t/helper/test-bundle-uri.c b/t/helper/test-bundle-uri.c
index 0329c56544f..25afd393428 100644
--- a/t/helper/test-bundle-uri.c
+++ b/t/helper/test-bundle-uri.c
@@ -4,12 +4,21 @@
 #include "strbuf.h"
 #include "string-list.h"
 
-static int cmd__bundle_uri_parse(int argc, const char **argv)
+enum input_mode {
+	KEY_VALUE_PAIRS,
+	CONFIG_FILE,
+};
+
+static int cmd__bundle_uri_parse(int argc, const char **argv, enum input_mode mode)
 {
 	const char *key_value_usage[] = {
 		"test-tool bundle-uri parse-key-values <input>",
 		NULL
 	};
+	const char *config_usage[] = {
+		"test-tool bundle-uri parse-config <input>",
+		NULL
+	};
 	const char **usage = key_value_usage;
 	struct option options[] = {
 		OPT_END(),
@@ -19,21 +28,35 @@ static int cmd__bundle_uri_parse(int argc, const char **argv)
 	int err = 0;
 	FILE *fp;
 
-	argc = parse_options(argc, argv, NULL, options, usage, 0);
-	if (argc != 1)
-		goto usage;
+	if (mode == CONFIG_FILE)
+		usage = config_usage;
+
+	argc = parse_options(argc, argv, NULL, options, usage,
+			     PARSE_OPT_STOP_AT_NON_OPTION);
 
 	init_bundle_list(&list);
-	fp = fopen(argv[0], "r");
-	if (!fp)
-		die("failed to open '%s'", argv[0]);
 
-	while (strbuf_getline(&sb, fp) != EOF) {
-		if (bundle_uri_parse_line(&list, sb.buf))
-			err = error("bad line: '%s'", sb.buf);
+	switch (mode) {
+	case KEY_VALUE_PAIRS:
+		if (argc != 1)
+			goto usage;
+		fp = fopen(argv[0], "r");
+		if (!fp)
+			die("failed to open '%s'", argv[0]);
+		while (strbuf_getline(&sb, fp) != EOF) {
+			if (bundle_uri_parse_line(&list, sb.buf))
+				err = error("bad line: '%s'", sb.buf);
+		}
+		fclose(fp);
+		break;
+
+	case CONFIG_FILE:
+		if (argc != 1)
+			goto usage;
+		err = bundle_uri_parse_config_format("<uri>", argv[0], &list);
+		break;
 	}
 	strbuf_release(&sb);
-	fclose(fp);
 
 	print_bundle_list(stdout, &list);
 
@@ -62,7 +85,9 @@ int cmd__bundle_uri(int argc, const char **argv)
 		goto usage;
 
 	if (!strcmp(argv[1], "parse-key-values"))
-		return cmd__bundle_uri_parse(argc - 1, argv + 1);
+		return cmd__bundle_uri_parse(argc - 1, argv + 1, KEY_VALUE_PAIRS);
+	if (!strcmp(argv[1], "parse-config"))
+		return cmd__bundle_uri_parse(argc - 1, argv + 1, CONFIG_FILE);
 	error("there is no test-tool bundle-uri tool '%s'", argv[1]);
 
 usage:
diff --git a/t/t5750-bundle-uri-parse.sh b/t/t5750-bundle-uri-parse.sh
index fd142a66ad5..c2fe3f9c5a5 100755
--- a/t/t5750-bundle-uri-parse.sh
+++ b/t/t5750-bundle-uri-parse.sh
@@ -118,4 +118,54 @@ test_expect_success 'bundle_uri_parse_line() parsing edge cases: duplicate lines
 	test_cmp_config_output expect actual
 '
 
+test_expect_success 'parse config format: just URIs' '
+	cat >expect <<-\EOF &&
+	[bundle]
+		version = 1
+		mode = all
+	[bundle "one"]
+		uri = http://example.com/bundle.bdl
+	[bundle "two"]
+		uri = https://example.com/bundle.bdl
+	[bundle "three"]
+		uri = file:///usr/share/git/bundle.bdl
+	EOF
+
+	test-tool bundle-uri parse-config expect >actual 2>err &&
+	test_must_be_empty err &&
+	test_cmp_config_output expect actual
+'
+
+test_expect_success 'parse config format edge cases: empty key or value' '
+	cat >in1 <<-\EOF &&
+	= bogus-value
+	EOF
+
+	cat >err1 <<-EOF &&
+	error: bad config line 1 in file in1
+	EOF
+
+	cat >expect <<-\EOF &&
+	[bundle]
+		version = 1
+		mode = all
+	EOF
+
+	test_must_fail test-tool bundle-uri parse-config in1 >actual 2>err &&
+	test_cmp err1 err &&
+	test_cmp_config_output expect actual &&
+
+	cat >in2 <<-\EOF &&
+	bogus-key =
+	EOF
+
+	cat >err2 <<-EOF &&
+	error: bad config line 1 in file in2
+	EOF
+
+	test_must_fail test-tool bundle-uri parse-config in2 >actual 2>err &&
+	test_cmp err2 err &&
+	test_cmp_config_output expect actual
+'
+
 test_done
