But if the president's candidate is rejected twice, he can then dissolve the rebellious legislature and appoint his own choice as acting governor.
Critics say the legislation returns Russia to the Soviet era, when the Kremlin appointed local Communist Party bosses. Critics also say it ends a major part of Russia's decade-long experiment with decentralization and undermines the country's status as a federation, which is stipulated in the constitution.
And it all happened on Russia's Constitution Day -- a bitter irony, according to legal experts.
Meeting yesterday in Moscow, the leaders of two marginalized liberal factions urged supporters to unite in the face of what they called Putin's growing authoritarianism. Boris Nemtsov, head of the Union of Right Forces, described the challenge: "The question is, Can civil society in Russia defend the freedom and democracy for which we fought so hard? The answer depends on whether democratic forces will be able to surmount their disunity or not."
His colleague, Grigorii Yavlinskii, agreed. The leader of the Yabloko faction said Russia's current rulers have no faith in democracy and it is up to the people and the opposition to remind them that democracy matters to them.
But such calls carry less weight in today's Russia than several years ago. Nemtsov and Yavlinskii both head parties that failed to make it into parliament during last year's elections. Their popularity ratings are in the single digits.
Across town, 15,000 Kremlin supporters -- members of pro-Putin youth group Walking Together -- gathered to show their support for the new law. Their leader, Vasilii Yakimenko, had a message for Yavlinskii and Nemtsov.
"When 18 people gather, who feel they represent someone, then somewhere else, 18,000 others must gather to tell them: 'You 18 people don't represent the nation. The whole nation stands with us,'" Yakimenko said.
Stephan De Spiegeleire, a Russia analyst at the RAND Europe think tank in the Netherlands, told RFE/RL that right now, Yakimenko and his supporters closely reflect the mood of the country. At a time of relative economic stability and fear of terrorism, Putin's approval ratings remain at over 70 percent. The overwhelming majority of Russians appear willing to trade in democratic reforms for a feeling of security.
De Spiegeleire said that the lack of debate in parliament over these major changes is indicative not only of the Kremlin's degree of control over those institutions, but of the current popular mood:
"This is an incredibly important change in the political structure of Russia. And the Duma and the Federation Council -- the two chambers of parliament in Russia -- accepted these changes with incredible speed, without the kind of debate that you would expect in such a society," de Spiegeleire said. "Now there are still representatives of both the left and the right in the Duma, but their voices are just not strong enough to be heard and to be translated into the political system."
Although experts have challenged the legality of the new measures, which would seem to contradict the division of powers envisaged by Russia's federative status, the Constitutional Court itself has stayed mum.
"This is so blatantly a violation of the Russian Constitution that you would at least expect the Constitutional Court to come up with some criticism," de Spiegeleire said. "And they're not."
Regional leaders, whose power will be directly undercut by the new law, are also refraining from criticism. All checks on the Kremlin's ambitions would seem to be absent.
When the Kremlin first introduced its bill in parliament in September, outspoken Duma Deputy Sergei Glazev said Putin was deluding himself if he believed that tightening central control -- the "vertical of power," as the Kremlin calls it -- would make the country stronger.
"A strong government gets its strength from the people, from self-government. In order to make the government healthier, to clear it of corruption, it is essential to introduce a mechanism of public control," Glazev said. "It is essential to make the government transparent, responsible and understandable. Clear guidelines defining its powers must be introduced. Other than elections, mankind has not invented any other mechanism to get incompetent and irresponsible people out of government, because the people are the most objective judge of the government. If the government rejects this judge, it becomes unaccountable."
De Spiegeleire said that as long as oil prices stay high and the economy continues to grow, the opposition will remain weak and voiceless. But should things change, he said, Putin's centralized structure could become his Achille's heel.
"I don't think right now there is a background in Russia for this popular outcry against the taking back of a lot of the democratic achievements that had been won under Yeltsin," de Spiegeleire said. "It's just not there -- not in the short term. I do think, however, that what is underappreciated by the Russian leadership is how fragile such a system is -- the system that is being created now, where ultimately one person is responsible, where the Kremlin gets more and more power and where there are hardly any checks and balances."
(RFE/RL's Russian Service contributed to this report)