Churkin, 64, was working at his desk when he collapsed, he was rushed to New York-Presbyterian/Columbia University Medical Center in New York, where he died, Russia's deputy UN ambassador, Vladimir Safronkov, told reporters. His cause of death wasn't immediately known.
Churkin had been Russia's envoy at the United Nations since 2006 and was considered Moscow's great champion at the UN, he had a reputation for an acute wit and sharp repartee, especially with his American and Western counterparts.
Churkin was a fierce defender of his country's policies, including Russia's invasion of Ukraine and its much-criticized bombing last year of the Syrian city of Aleppo to oust rebels opposed to President Bashar Al-Assad.
Russia's foreign ministry called Churkin an "outstanding" diplomat and expressed condolences to his friends and family. Born Feb. 21, 1952, in Moscow, Churkin died a day before his 65th birthday.
"Our thoughts go to his family, to his friends and to his government,'' said UN deputy spokesman Farhan Haq, who heard the news from reporters as it circulated during a daily briefing.
According to a U.N. biography, Churkin began his 42-year diplomatic career in 1974 when Russia was still the driving force of the Soviet Union.
Churkin was previously ambassador at large and earlier served as the foreign ministry spokesman. Churkin had a doctorate in history and was a graduate of the Moscow State Institute of International Relations.
Fluent in English and French, Churkin was a child actor who appeared in pair of Communist-era movies about V.I. Lenin before he set out to become a diplomat.