The monastery was founded in 1444 by the venerable Pafnutiy Borovskiy on a hill at the confluence of the Istrema and Protva rivers. Its creation is linked to the Mongol-Tatar invasion: Pafnutiy's grandfather, a Tatar, converted to Orthodoxy under the name Martin, becoming the founder of a pious lineage from which the future "lamp" of faith emerged. After Pafnutiy's death, the monastery was led by his disciple, the venerable Joseph of Volokolamsk, who, finding no support among the brethren for adopting a communal rule, founded the Joseph-Volokolamsk Monastery.

In 1467, a white-stone Nativity Cathedral was built on the site of the first wooden church, which has not survived. The painting of this cathedral became the first known work of the great icon painter Dionysius, completed under the guidance of the elder of the Simonov Monastery, icon painter Mitrophan.

In 1586, the cathedral was almost completely dismantled, and a new five-domed church was built in its place by order of Tsar Fyodor Ivanovich, incorporating blocks with 15th-century frescoes into its foundation. Fragments of the frescoes by Mitrophan and Dionysius have survived and are housed in the Central Museum of Ancient Russian Culture and Art named after Andrei Rublev in Moscow and the Borovsk branch of the Kaluga State Regional Local Lore Museum.

In the 16th century, the monastery was surrounded by stone walls and fortifications, transforming it into a powerful border fortress. At that time, a stone refectory with the Church of the Nativity of Christ was built, and in 1523, a bell tower.

The spiritual authority of Pafnutiy attracted many people to the monastery. Grand Dukes Vasily II, Ivan III, Vasily III, Tsars Ivan IV the Terrible, Fyodor Ivanovich, Mikhail Romanov, and Alexei Mikhailovich, as well as Princes Lykov-Obolensky, Repnins, and Volkonskys, often visited the monastery for prayer.

During the Time of Troubles, the monastery found itself in the path of Polish-Lithuanian invaders led by False Dmitry II and became the site of bloody events, the heroism of the defenders remaining in history, while the city of Borovsk received a new coat of arms. The monastery was also affected by the events of the church schism: Protopope Avvakum, the inspirer of the old church order, was held here under guard twice.

In 1812, during the war with Napoleon, the monastery was looted and partially destroyed. The Great Patriotic War of 1941-1945 also left its mark on its history: the monastery suffered again but managed to revive. During the Soviet period, the monastery experienced its most difficult times: after nationalization and the expulsion of monks in 1919, it was almost destroyed.

Restoration began in the 1960s when restorers faced numerous difficulties: new foundations had to be poured, walls restored, and churches renovated.

The modern history of the monastery began in 1991 with the return of monks and the resumption of regular services. Today, the monastery is active: services are held daily in its churches, the number of residents is increasing, and forms of social service are being improved.