In the early 17th century, a wooden church with the same name stood on the site of the stone Annunciation church. In 1678, another warm church was built next to it. Comparing data from 1646 and 1678, it can be assumed that the cold cathedral church was reconstructed during this period, as the chapel of Saint Martyr Paraskeva, which was located at the Annunciation church in 1646, by 1678 belonged to the warm church of the Beheading of John the Baptist.

By the end of the 17th century, a stone cathedral was built to replace the wooden Annunciation church, consecrated in 1700. Its founder was merchant Semyon Yershov. The church, which has five domes, has preserved its original exterior appearance to this day, although the interior decoration has been significantly updated recently. The church has two altars: the main one in honor of the Annunciation of the Blessed Virgin Mary, and in the chapel, in honor of the Venerable Macarius of Yellow Waters, established in 1864 in memory of the chapel of the same name in the wooden church.

Next to the cold cathedral church is a stone warm church, but information about the time and author of its construction has not survived. It has one dome and is divided inside into three parts by two transverse arches: the altar, the church itself, and the refectory. This church also has two altars: the main one in honor of the Beheading of Saint John the Baptist, and in the chapel, in honor of Saint Martyr Paraskeva. Separate from the churches stands a stone bell tower with a tented top, the time of its construction is unknown. Both cathedral churches have preserved several ancient icons and other sacred items.

In the Annunciation church, the ancient Smolensk icon of the Mother of God is especially venerated, considered miraculous, with a silver and partially gilded robe. In the warm cathedral church, notable for their antiquity are the icons: the local icon of the Almighty, painted in 1659, the church icon of Saint John the Baptist from 1628, the icon of Saint Nicholas the Wonderworker, as well as the icons of Saints Alexius the Man of God and Mary of Egypt, painted in 1652.

Since 1870, the Sretenskaya church of the former women's monastery and the cemetery church of All Saints have been attributed to the Annunciation Cathedral.