diff --git a/doc/man1/notmuch-config.rst b/doc/man1/notmuch-config.rst
index 223d2de5..32290a38 100644
--- a/doc/man1/notmuch-config.rst
+++ b/doc/man1/notmuch-config.rst
@@ -7,7 +7,7 @@ SYNOPSIS
 
 **notmuch** **config** **get** <*section*>.<*item*>
 
-**notmuch** **config** **set** <*section*>.<*item*> [*value* ...]
+**notmuch** **config** **set** [--database] <*section*>.<*item*> [*value* ...]
 
 **notmuch** **config** **list**
 
@@ -30,6 +30,10 @@ configuration file and corresponding database.
     If no values are provided, the specified configuration item will
     be removed from the configuration file.
 
+    With the `--database` option, updates configuration metadata
+    stored in the database, rather than the default (text)
+    configuration file.
+
 **list**
     Every configuration item is printed to stdout, each on a separate
     line of the form::
diff --git a/doc/man1/notmuch.rst b/doc/man1/notmuch.rst
index fecfd08a..48351588 100644
--- a/doc/man1/notmuch.rst
+++ b/doc/man1/notmuch.rst
@@ -48,7 +48,9 @@ Supported global options for ``notmuch`` include
 
 ``--config=FILE``
     Specify the configuration file to use. This overrides any
-    configuration file specified by ${NOTMUCH\_CONFIG}.
+    configuration file specified by ${NOTMUCH\_CONFIG}. The empty
+    string is a permitted and sometimes useful value of *FILE*, which
+    tells ``notmuch`` to use only configuration metadata from the database.
 
 ``--uuid=HEX``
     Enforce that the database UUID (a unique identifier which persists
diff --git a/notmuch-config.c b/notmuch-config.c
index 24c16833..c4283576 100644
--- a/notmuch-config.c
+++ b/notmuch-config.c
@@ -511,16 +511,15 @@ validate_field_name (const char *str)
 
 typedef struct config_key {
     const char *name;
-    bool in_db;
     bool prefix;
     bool (*validate)(const char *);
 } config_key_info_t;
 
 static struct config_key
     config_key_table[] = {
-    { "index.decrypt",   true,   false,  NULL },
-    { "index.header.",   true,   true,   validate_field_name },
-    { "query.",          true,   true,   NULL },
+    { "index.decrypt",   false,  NULL },
+    { "index.header.",   true,   validate_field_name },
+    { "query.",          true,   NULL },
 };
 
 static config_key_info_t *
@@ -583,11 +582,36 @@ _set_db_config (notmuch_database_t *notmuch, const char *key, int argc, char **a
 }
 
 static int
-notmuch_config_command_set (notmuch_config_t *config, notmuch_database_t *notmuch, char *item,
+notmuch_config_command_set (notmuch_config_t *config, notmuch_database_t *notmuch,
 			    int argc, char *argv[])
 {
     char *group, *key;
     config_key_info_t *key_info;
+    bool update_database = false;
+    int opt_index;
+    char *item;
+
+    notmuch_opt_desc_t options[] = {
+	{ .opt_bool = &update_database, .name = "database" },
+	{ }
+    };
+
+    opt_index = parse_arguments (argc, argv, options, 1);
+    if (opt_index < 0)
+	return EXIT_FAILURE;
+
+    argc -= opt_index;
+    argv += opt_index;
+
+    if (argc < 1) {
+	fprintf (stderr, "Error: notmuch config set requires at least "
+		 "one argument.\n");
+	return EXIT_FAILURE;
+    }
+
+    item = argv[0];
+    argv++;
+    argc--;
 
     if (STRNCMP_LITERAL (item, BUILT_WITH_PREFIX) == 0) {
 	fprintf (stderr, "Error: read only option: %s\n", item);
@@ -598,7 +622,7 @@ notmuch_config_command_set (notmuch_config_t *config, notmuch_database_t *notmuc
     if (key_info && key_info->validate && (! key_info->validate (item)))
 	return 1;
 
-    if (key_info && key_info->in_db) {
+    if (update_database) {
 	return _set_db_config (notmuch, item, argc, argv);
     }
 
@@ -692,12 +716,7 @@ notmuch_config_command (notmuch_config_t *config, notmuch_database_t *notmuch,
 	}
 	ret = notmuch_config_command_get (notmuch, argv[1]);
     } else if (strcmp (argv[0], "set") == 0) {
-	if (argc < 2) {
-	    fprintf (stderr, "Error: notmuch config set requires at least "
-		     "one argument.\n");
-	    return EXIT_FAILURE;
-	}
-	ret = notmuch_config_command_set (config, notmuch, argv[1], argc - 2, argv + 2);
+	ret = notmuch_config_command_set (config, notmuch, argc, argv);
     } else if (strcmp (argv[0], "list") == 0) {
 	ret = notmuch_config_command_list (notmuch);
     } else {
diff --git a/test/T030-config.sh b/test/T030-config.sh
index c87d35b6..b22d8f29 100755
--- a/test/T030-config.sh
+++ b/test/T030-config.sh
@@ -124,4 +124,24 @@ count=$(notmuch count '*')
 test_expect_equal "${path} ${count}" \
 		  "Maildir 52"
 
+test_begin_subtest "Add config to database"
+notmuch new
+key=g${RANDOM}.m${RANDOM}
+value=${RANDOM}
+notmuch config set --database ${key} ${value}
+notmuch dump --include=config > OUTPUT
+cat <<EOF > EXPECTED
+#notmuch-dump batch-tag:3 config
+#@ ${key} ${value}
+EOF
+test_expect_equal_file EXPECTED OUTPUT
+
+test_begin_subtest "Roundtrip config to/from database"
+notmuch new
+key=g${RANDOM}.m${RANDOM}
+value=${RANDOM}
+notmuch config set --database ${key} ${value}
+output=$(notmuch config get ${key})
+test_expect_equal "${output}" "${value}"
+
 test_done
diff --git a/test/T600-named-queries.sh b/test/T600-named-queries.sh
index 0ae8b83d..a7b84995 100755
--- a/test/T600-named-queries.sh
+++ b/test/T600-named-queries.sh
@@ -4,13 +4,13 @@ test_description='named queries'
 
 QUERYSTR="date:2009-11-18..2009-11-18 and tag:unread"
 
-test_begin_subtest "error adding named query before initializing DB"
-test_expect_code 1 "notmuch config set query.test \"$QUERYSTR\""
+test_begin_subtest "error adding named query to DB before initialization"
+test_expect_code 1 "notmuch config set --database query.test \"$QUERYSTR\""
 
 add_email_corpus
 
-test_begin_subtest "adding named query"
-test_expect_success "notmuch config set query.test \"$QUERYSTR\""
+test_begin_subtest "adding named query (database)"
+test_expect_success "notmuch config set --database query.test \"$QUERYSTR\""
 
 test_begin_subtest "adding nested named query"
 QUERYSTR2="query:test and subject:Maildir"
@@ -32,7 +32,6 @@ test_begin_subtest "dump named queries"
 notmuch dump | grep '^#@' > OUTPUT
 cat<<EOF > QUERIES.BEFORE
 #@ query.test date%3a2009-11-18..2009-11-18%20and%20tag%3aunread
-#@ query.test2 query%3atest%20and%20subject%3aMaildir
 EOF
 test_expect_equal_file QUERIES.BEFORE OUTPUT
 
@@ -40,23 +39,21 @@ test_begin_subtest 'dumping large queries'
 # This value is just large enough to trigger a limitation of gzprintf
 # to 8191 bytes in total (by default).
 repeat=1329
-notmuch config set query.big "$(seq -s' ' $repeat)"
+notmuch config set --database query.big "$(seq -s' ' $repeat)"
 notmuch dump --include=config > OUTPUT
-notmuch config set query.big ''
+notmuch config set --database query.big
 printf "#notmuch-dump batch-tag:3 config\n#@ query.big " > EXPECTED
 seq -s'%20' $repeat >> EXPECTED
 cat <<EOF >> EXPECTED
 #@ query.test date%3a2009-11-18..2009-11-18%20and%20tag%3aunread
-#@ query.test2 query%3atest%20and%20subject%3aMaildir
 EOF
 test_expect_equal_file EXPECTED OUTPUT
 
 test_begin_subtest "delete named queries"
 notmuch dump > BEFORE
-notmuch config set query.test
+notmuch config set --database query.test
 notmuch dump | grep '^#@' > OUTPUT
 cat<<EOF > EXPECTED
-#@ query.test2 query%3atest%20and%20subject%3aMaildir
 EOF
 test_expect_equal_file EXPECTED OUTPUT
 
diff --git a/test/T750-user-header.sh b/test/T750-user-header.sh
index 586788b3..05f80885 100755
--- a/test/T750-user-header.sh
+++ b/test/T750-user-header.sh
@@ -2,14 +2,6 @@
 test_description='indexing user specified headers'
 . $(dirname "$0")/test-lib.sh || exit 1
 
-test_begin_subtest "error adding user header before initializing DB"
-notmuch config set index.header.List List-Id 2>&1 | notmuch_dir_sanitize > OUTPUT
-cat <<EOF > EXPECTED
-notmuch config: Illegal argument for function
-Cannot reopen closed or nonexistent database
-EOF
-test_expect_equal_file EXPECTED OUTPUT
-
 add_email_corpus
 
 notmuch search '*' | notmuch_search_sanitize > initial-threads