On August 7, 1314, Archbishop Prokhor of Rostov miraculously discovered an icon of the Mother of God on the banks of the Volga. News of this event quickly spread to Yaroslavl, where many people of different classes and ages arrived. With collective efforts, a church was built in half a day, and by evening Archbishop Prokhor consecrated it in the name of the Introduction of the Mother of God into the Temple. He brought in the icon, named Tolga after the small river Tolga that flows into the Volga, and established an annual celebration of the icon's appearance on August 8. On the same day, Prokhor announced the creation of the monastery and appointed its abbot.

Throughout its history, the monastery has been visited by historical figures such as Tsar Ivan the Terrible, Empress Catherine II, and Emperor Nicholas II. The monastery gradually expanded and underwent reconstruction.

Initially, the Tolga Monastery was male, but it was closed by the Soviet authorities in 1928. It was only reopened in December 1987, becoming the first female monastery in the RSFSR.