In a highly choreographed joint interview with state television after attending a ballet together, Putin's wife Lyudmila said they were having a "civilised divorce" and revealed that the pair hardly ever saw each other.
Lyudmila said she was grateful to Putin for supporting her, while Putin praised the fact she had "stood guard" for the almost nine years he has served as president.
"We are always going to be very close to each other. I am sure, forever," said the Russian strongman.
The announcement unleashed speculation about whether Putin is seeing another woman, a subject that has so far been taboo.
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Putin's spokesman Dmitry Peskov denied the 60-year-old president was planning to remarry, telling the Echo of Moscow radio station: "I can say for sure that this is more about rumours and tittle-tattle."
The Moskovsky Korrespondent newspaper, owned by tycoon Alexander Lebedev, reported in 2008 that Putin was about to marry Olympic gymnast turned legislator Alina Kabayeva, 31 years his junior. The paper then denied its own story and was closed by its owner.
The reason for the timing of the announcement is unclear.
The carefully choreographed revelation may be aimed at improving Putin's image as a man wedded to his job at a time of challenges from opposition protests and increased Internet scrutiny of his life.
In May in a public phone-in, Putin said his work was his "whole life. I don't know if that is enough for happiness."
Lyudmila, 55, a former flight attendant, revealed in their interview that she disliked flying and was averse to publicity, factors that had made the marriage impossible.
His spokesman said the couple had not yet filed for divorce, asking for respect for their privacy.
Today, the story dominated the Internet, with many praising Putin for speaking frankly.