The Holy Assumption Monastery in Dunilovo was founded in the late 17th century by boyar Fyodor Abramovich Lopukhin, the father of Tsarina Evdokia. With his funds, the Assumption communal male Hermitage was built in the floodplain of the Teza River, on the outskirts of Dunilovo, previously known as Dubnilovo, featuring two wooden churches dedicated to the Assumption and Protection of the Mother of God. In 1725, the Assumption Hermitage was annexed to the Yuriev-Polsky Archangel Monastery and later transferred to the Holy Nicholas-Shartom Monastery. In 1764, during the church reform under Catherine II, the Hermitage was abolished, its property transferred to the Dunilovo Annunciation Women's Monastery, and the wooden structures burned down.

In the early 19th century, two stone churches were built on the site of the former hermitage with the previous altars. The summer Assumption church was consecrated in 1819, and the winter Protection church in 1848. The Assumption church had three altars: in honor of the Assumption of the Mother of God, the Merciful Savior, and the Nativity of the Most Holy Theotokos. The church housed the miraculous icon of the Mother of God of Smolensk. The architecture of the Assumption church is unique, combining classical forms with elements of baroque. The massive rotunda, located on the quadrangle of the main volume of the church with a high spherical roof, is topped with five slender drums with elegant domes.

After the revolution, both churches were closed. During the Soviet era, the territory of the former monastery housed a psycho-neurological boarding school: the Protection church was converted into a hospital ward, and a treatment room was arranged in the altar, while the Assumption church was used as a warehouse. In 1991, a communal women's monastery was established in honor of the Assumption of the Mother of God on the site of the former Assumption Hermitage. Restoration began with the Protection church, followed by the restoration of the heavily damaged Assumption church. In the summer of 1995, domes were raised on the bell tower, and in 1996, the main 16-pud bell, brought from Tutayev, was installed.

In 1997, on the feast of the Assumption, the first service was held in the church. Since then, services have been conducted on the feast day, while the church remains closed for restoration at other times. Of the 12 churches that existed in Dunilovo before the revolution, ten survived. In 1995, by the decree of Archbishop Ambrose of Ivanovo and Kineshma, all the churches of the village of Dunilovo were transferred to the management of the Holy Assumption Women's Monastery.