The Church of the Nativity of John the Baptist in the Blagoveshchenskaya Sloboda was founded in the 15th century. According to legend, Kuzma Minin lived in the parish of the church until 1612. The wooden church burned down in the fire of 1715, but thanks to the efforts of the parishioners, a stone church was built from 1721 to 1725. It was reconstructed in 1876.

The church was located in Blagoveshchenskaya Sloboda, near the Blagoveshchensky Monastery and the Romodanovsky Station, on a street now called Chernigovskaya. According to legend, the residents of the sloboda erected a chapel at the site of the execution of the robber Suleika. In the 15th century, the chapel was transformed into a church in honor of Saint John the Baptist. In documents from 1621 and 1622, it is mentioned as an old church.

In the fire of 1715, the wooden Vvedenskaya Church also burned down along with the church. In their place, from 1721 to 1725, under Archbishop Pitirim, the stone Preobrazhenskaya Church was built. The altars in the church were consecrated in memory of the previous churches: the main one in honor of the Entry into the Temple of the Most Holy Theotokos, and the side altars in the refectory, in honor of the Nativity of John the Baptist and All Saints.

Maria Ivanovna Khlopova, the fiancée of Tsar Mikhail Fyodorovich and a parishioner of the church, was buried in the churchyard. The church housed the miraculous icon of the Mother of God "Cyprus," which stopped an epidemic in 1771.

On November 21, 1918, an agreement was concluded for the use of the church building, which listed 275 members of the community. On July 25, 1928, the Nizhgorov Soviet decided to close the church and convert it into a workers' club. On September 10, 1928, a special commission inspected the building and found cracks indicating the detachment of the altar. The commission ruled that restoring the building would require significant funds and was impractical, so the church was dismantled. The representative of the believers did not object to this decision.

In 1983, the building was significantly reconstructed for administrative needs. The bell tower and part of the refectory were preserved, which became part of a three-story administrative building housing the Committee for Environmental Protection and Natural Resources of the Nizhny Novgorod Region. Currently, restoration of the remaining part of the church is underway to recreate its original appearance.