The Slobodsk-Blagoveshchensk church was founded in 1619. By the end of the 19th century, its parish had 344 households with a population of 2,829 people. In 1641, Blagoveshchensk received the status of a town and included 46 of the best tribute-paying households. By the end of the 17th century, there were 53 households, 45 barns, and three churches: a church in honor of Florus and Laurus, built in 1647; the tent-roofed Blagoveshchensk church, erected in 1664; and the nine-domed Transfiguration church, built in 1683.

In July 1806, the Blagoveshchensk and Transfiguration churches were destroyed by lightning. From 1807 to 1817, a new stone church was built in their place. It was a two-story five-domed building with four altars: Transfiguration, Peter and Paul, as well as the lower Blagoveshchensk and Evdokia altars. The church was surrounded by a fence made of cast iron decorative casting.

In 1929, the church was closed, and its premises were partially used as a club, bakery, and store. After a fire in 1962, the club was permanently moved to the neighboring wooden Alexander Nevsky church. Currently, part of the church has been returned to the faithful and is used for services. Parishioners are engaged in the reconstruction of the building.