Russia's state space corporation, Roskosmos, said it had lost contact with the craft shortly after a problem occurred as the craft was shunted into pre-landing orbit on Saturday.
"The apparatus moved into an unpredictable orbit and ceased to exist as a result of a collision with the surface of the Moon," Roskosmos said in a statement.
Failure for the prestige mission underscores the decline of Russia's space power since the glory days of Cold War competition when Moscow was the first to launch a satellite to orbit the Earth - Sputnik 1, in 1957 - and Soviet cosmonaut Yuri Gagarin became the first man to travel into space in 1961.
Russia has not attempted a moon mission since Luna-24 in 1976, when Leonid Brezhnev ruled the Kremlin. Luna-25 was supposed to execute a soft landing on the south pole of the moon on Aug. 21, according to Russian space officials.
Russia has been racing against India, whose Chandrayaan-3 spacecraft is scheduled to land on the moon's south pole this week, and more broadly against China and the United States which both have advanced lunar ambitions.