Its founder, St. Cyril or Kirill of Beloozero, following the advice of his teacher, St. Sergius of Radonezh, first dug a cave here, then built a wooden Dormition chapel and a loghouse for other monks.

Being a member of the influential Velyaminov clan of boyars, Kirill relinquished the office of father superior of the greatest cloister in medieval Moscow, the Simonov monastery.

It seems that the Muscovite rulers regarded Kirill's monastery as an important strategic point, both for Northern trade and in their struggle with the Novgorod Republic.

Among the Muscovite politicians exiled to Kirillov were Vassian Patrikeyev, Tsar Simeon Bekbulatovich, Patriarch Nikon, and the prime minister Boris Morozov.

Although the tsar chastised them for having broken canonical requirements, the chapel — which became the first family mausoleum in Russia — survived Ivan's reign and was expanded to its present form in 1623.

The first construction works were supervised by Jean de Gron, a French military engineer known in Russian sources as Anton Granovsky.

After the monastic authorities denigrated his Western-style design as alien to Russian traditions, Granovsky was replaced by a team of native masters.

After the Bolsheviks, the monastery was secularised and turned into a museum (1924), a wooden shrine from 1485 and several traditional timber structures were put on exhibit on the grounds.