The first wooden church dedicated to the Equal-to-the-Apostles Myrrh-bearing Women was built in 1566. The stone five-domed temple was constructed from 1714 to 1722 with funds from parishioner, merchant Pyotr Rodionov Khudyakov, as confirmed by the church inventory of 1764. The temple was consecrated on July 12, 1724. According to the description of the Sretensky Cathedral by A. Popov, published in the "Vologda Diocesan Gazette" of 1875, the construction of the stone church began in 1710. He mentions that on the western wall of the church of the Myrrh-bearing Women there is an inscription: "The beginning of the building of this church in the year 1710."

In the refectory iconostasis, there were icons of: the Almighty with John the Baptist, Saint Nicholas the Wonderworker, the Mother of God on the throne with the guardian angel, and 46 Pechora saints, as well as Saint Martyr Haralampius.

Among the church utensils stands out a pectoral cross with 12 relics of saints, including the Apostle Andrew the First-Called, Archdeacon Stephen, Basil the Great, John the Merciful, Great Martyr Theodore Stratilates, Martyr Panteleimon, and others. Inside the cross on cypress, where the relics are placed, their names are indicated, and an inscription has been preserved: "In the year 7193, these holy relics were placed in this holy cross in the reigning city of Moscow, in the Annunciation Cathedral, at the old gates in the vestibule, by Priest John, for the glory of the Holy Trinity and the Most Pure Mother of God." On the reverse side of the cross, it is written: "In the year 7193, this holy Lord's cross was constructed by the efforts of guest Semyon Khrisanthov, son of Shilovtsov, and his wife Martha Terentyeva's daughter, in the city of Veliky Ustyug, in the settlement for the Church of the Vladimir Mother of God and the holy Myrrh-bearing Women."

The church in the name of the Myrrh-bearing Women was closed in February 1930. Currently, its walls house the "Museum of New Year Toys," which is a branch of the Veliky Ustyug Museum-Reserve.