The monastery, founded by Saint Ferapont in 1398, has a rich history. Ferapont, from the noble family of Paskochins, became a monk at the Simonov Monastery in Moscow. Together with his friend, Saint Kirill of Belozersk, he went North but decided to establish his own monastery 15 km from the Kirillo-Belozersky Monastery. Like Kirill, Ferapont soon was no longer alone; the number of monks increased, they built cells, and in 1409 erected a wooden church of the Nativity of the Mother of God and a refectory. Thanks to the Venerable Martinian of Belozersk, who became the abbot at the request of the brethren, Ferapont's monastery gained fame.

The monastery became a place of pilgrimage and donations from the Russian nobility, alongside the Kirillo-Belozersky Monastery. In the late 15th and early 16th centuries, significant hierarchs of the Russian church emerged from its walls, such as Archbishop Joasaph of Rostov and Yaroslavl, Bishops Philotheus of Perm and Vologda, and Ferapont of Suzdal. Here worked scribes Martinian, Spiridon, Philotheus, Paisius, Matthew, Ephrosin, and icon painter Dionysius. The Venerable Kassian the Greek, who arrived in Russia with Sophia Palaiologina, was also a monk of the monastery. In the 16th century, the monastery flourished, as confirmed by donation and charter grants, including from Ivan IV. Pilgrims included Vasily III, Elena Glinskaya, and Ivan IV. The donation book of 1534 mentions among the donors the princes of Staritsky, Kubensky, Lykov, Belsky, Shuisky, Vorotynsky, Godunov, Sheremetyev, and others, as well as bishops from Siberia, Rostov, Vologda, Belozersk, and Novgorod.

After the discovery of the relics of the Venerable Martinian and his canonization, the monastery attracted more attention and donations. In 1490, the construction of a stone ensemble with the Cathedral of the Nativity of the Mother of God began. In the 16th century, the Church of the Annunciation with a refectory, a treasury, service buildings, and other structures were built.

In 1798, the monastery was closed by the Synod's decree, and its churches became parish churches. In the 19th century, the monastery's territory was enclosed with a stone fence. In 1904, the monastery was restored as a women's monastery but was closed again in 1924.

Since 1975, the creation of a museum began, which became a scientific and educational center promoting the unique monuments of the monastery. From 2012 to 2018, conservation work was carried out to preserve the frescoes of Dionysius. In 2019, the Moscow Patriarchate reported the completion of work to preserve the monumental painting of the 16th century.