The couple looked nervous as they stood side by side in the Kremlin, speaking to a lone reporter. They referred to each other formally by first name and patronymic, adding a respectful but uncomfortable touch.
Putin smiled woodenly and nodded as Lyudmila spoke, though they both appeared more relaxed after making the announcement.
Lyudmila, a former airline stewardess five years younger than the 60-year-old president, said it had been "our common decision".
"Our marriage is over due to the fact that we barely see each other," she said. Putin also said it had been "a joint decision".
The Putins married in 1983 and have two daughters, both in their 20s. The announcement came 13 months into a third presidential term for Putin, who came to power in 2000 and has not ruled out seeking re-election in 2018.
The couple have made only rare, sometimes awkward, appearances together over recent years, prompting media speculation that they had secretly divorced.
In 2008, Putin said there was no truth to a newspaper report that he was preparing to marry Olympic rhythmic gymnast Alina Kabayeva, who was born the same year he married Lyudmila.
Putin told journalists to keep their "snotty noses" out of his private life and the newspaper folded shortly afterwards. Kabayeva has dismissed speculation she had a child by Putin.
"DONE HER SHIFT"
The Putins spoke to Rossiya-24 TV after attending a ballet performance in the Kremlin, in what at first appeared to be a staged effort to show that they were still together.
After answering questions at length about the ballet, the Putins were asked about the rumors they lived apart.
Putin added: "Lyudmila Alexandrovna and I will always remain close - forever, I am sure."
Neither clarified whether their marriage was legally dissolved, although Lyudmila said it was a "civilized divorce". Putin's spokesman said he did not know.
"They separated a long time ago," Dmitry Peskov said. "I don't know if the divorce has been formalized, but I can confirm that we are talking about a civilized divorce."
Putin has made questions about his family taboo, jealously guarding information about his daughters, and it is highly unlikely the reporter asked the question without prompting. The remarks were first aired after prime time, after 9:30 p.m.
While the couple were widely assumed to be estranged, the unexpected admission set off a wave of comment on the Internet, a prominent platform for criticism of Putin in a nations whose mainstream broadcast media is controlled by the state.
"It's time for the whole country to divorce him," a group called For Honest Elections, which has used social network sites to help organize protests against Putin, said on its Twitter microblog.
Soviet and Russian leaders have faced little scrutiny over their family lives, and divorce is a fact of life. In 2011, about 1.3 million Russian couples marries and nearly 670,000 divorced, according to government figures.
Anna, a 26-year-old Muscovite who gave only her first name, praised Putin for a "good move".
"When (former French president Nicolas) Sarkozy announced his divorce, I thought to myself, 'This would just be impossible in this country.' And now look what's happening."
However, she thought it would not play well in the provinces, where Putin's main support base lies.
"I fear his ratings will go down further," she said of Putin, whose approval rating fell to a 12-year low of 62 percent in January according to the independent Levada Center, but has since edged up.
Boris Nemtsov, a prominent opposition politician and a leader of a series of protests against Putin and the ruling party in the past 18 months, said he did not believe the timing was driven by political considerations.
"I don't know why they announced it now, you'd better ask them. I can only say that even though lying all the time is Putin's tradition, the fact that he found the courage to announce his divorce is an honest deed," Nemtsov said.
"They have not been living together for a long time, everyone knew it. It is pleasant when someone behaves like an honest person, even though he may be your political rival."
(Editing by Mark Heinrich)