The Annunciation Church on Nikitskaya Street, located behind the Bolkhovka River, is first mentioned in the Land Book of 1624-1625, compiled by scribe Nikita Ivanovich Beklemishev and clerk Osip Trofimov. The document refers to a wooden church of the Annunciation of the Most Holy Theotokos with an altar dedicated to the martyr Christ's Nikita, which housed icons, books, bells, and other church property belonging to priest Stepan. There was also a cemetery, priests' yards, and three yards of widowers near the church. On September 21, 1661, the church burned down, but in the same year, Metropolitan Pitirim of Saransk and Podon issued a decree for the construction of a new church.

In 1730 (according to other sources, in 1740), a cold stone church was built on the site of the wooden church, with a warm Nikita altar in the refectory on the right. In 1760, a warm altar in honor of the martyrs Saint Cyricus and Julitta was arranged in the refectory on the left. In 1880, the old refectory was demolished and replaced with a more spacious one.

The church was closed in the 1930s. The completion of the church and the bell tower were dismantled after the Great Patriotic War. Under the crumbling plaster on the oldest part of the church, traces of beautiful window frames from the second quarter of the 18th century are visible, likely carved in 1880. Although the main volume of the church has been preserved, its current condition raises concerns.

The restoration project for the Annunciation Church in Bolkhov, the only one in the Oryol Diocese dedicated to this twelfth feast, was developed in the spring of 2015 in the Bolkhov Deanery. With the blessing of Metropolitan Antony of Oryol and Bolkhov, it is planned to first restore the lost bell tower. Currently, an asphalt road has been laid over its foundation, which historically did not exist.