The church is located on the site where wooden temples stood since the 13th century, which were repeatedly burned and restored. Initially, there were two wooden churches here: the cold Ascension of the Lord God and our Savior Jesus Christ, and the warm Epiphany of the Lord God and our Savior Jesus Christ. The current church was built in 1648 with funds from the Veliky Ustyug merchant Nikifor Revyakin. According to the census book from 1676-1683, by the end of the 17th century, the Ascension Church had eleven domes, of which only seven have survived to this day. The church is a complex multi-volume composition, likely resulting from several construction periods. It is known that in 1742, the altar apse was rebuilt. The main five-domed, pillarless church is square-shaped and covered with a vaulted ceiling adorned with decorative kokoshniks and a central light drum. It is surrounded on three sides by two-story chapels, and on the western side, there is an external stone staircase with landings. On the northern side, there is a two-story annex that wraps around the main volume, and to the west, where the bell tower rises, it forms a single whole with the church. The tower part of the bell tower, judging by its composition and details, appeared as a result of one of the reconstructions in the 18th century. On the southern side, an elegant annex adjoins the main church, topped with a dome on a double high drum. The external decoration of the church features various tiles, used for the first time in Ustyug.

The fire of 1715 destroyed the ancient utensils and the iconostasis with icons in the church. The existing carved gilded five-tiered iconostasis dates back to 1744, and the icons are works of mid-18th century painting. Once, an ancient wooden cross with a carved Crucifixion stood behind the altar. The iconostasis of the chapel contained an ancient image of the Mother of God of All Sorrows with a pearl robe. Many ancient images were placed above the doors and in the pilasters. A small four-tiered iconostasis also decorates the warm Resurrection Church. Its feature is the royal gates, divided into several panels with lace made of punched iron. The icons in the iconostasis also date back to the 18th century, some of them painted by the local icon painter Stepan Sokolov in 1719, shortly after the fire, and the icon of 'All Sorrows' in 1753. The Mother of God Odigitria of Smolensk, painted by Stepan Sokolov in 1718, comes from the local row of the iconostasis of the Resurrection chapel of the Ascension Church. The Dormition of the Mother of God, painted by Vasily Kolmogorov in 1744, also comes from the local row of the iconostasis of the Resurrection chapel of the Ascension Church.

On February 14, 1930, the Ascension Church was closed, and its property was divided among the State Fund, the museum, and the community of believers. The church building was transferred to the museum, but due to a lack of security, it was subjected to vandalism. Windows were broken, and cracks appeared in the walls. In 1933, the building experienced two fires, damaging the entrance doors, the coverings of the drums and the bell tower. Inside the building, icons were removed from the iconostases and scattered, some had their copper robes taken off, and part of the carving was destroyed. The church library was scattered in the altar, the chandelier was damaged, and the iconostasis of the upper church was affected. A beautiful colored tiled stove from the 18th century was destroyed. In June 1934, N.G. Bekryashev demanded that the city council carry out repairs on the building and organize its permanent security. In May 1937, he raised the issue of the church's security and repairs again. Thanks to the efforts of N.G. Bekryashev, it was possible to stop the destruction of the Ascension Church and begin its restoration.