The first mention of the wooden church dates back to 1618, and it was then called Alexeyevskaya. During a storm on May 26, 1698, the church burned down, and the nearby bell tower was cut down due to its proximity to the fire. The stone church was laid on May 23, 1710, and from 1728 it was called the Ioannopredtechenskaya. In 1930, an anti-religious museum opened in the church building, and later a children's theater was located there.

The wall paintings date back to 1717, according to a fragment of an inscription on the southern wall, but the author of the paintings is unknown. Researchers suggest that they were created by Yaroslavl masters, possibly under the guidance of the banner painter Fyodor Ignatiev, a student of Dmitry Plekhanov. The Pretechenskaya paintings are monuments of late monumental church painting, combining traditions of the 17th century with Western Baroque influences.

In the dome of the temple, there is an image of the "Fatherland," and on the octagonal vault, a series of compositions of the "Symbol of Faith" is located. The upper registers of the painting are dedicated to the earthly life of Christ, followed by scenes of the apostolic deeds and the martyrdom of the apostles. The walls of the square are detailed with the life of St. John the Baptist and compositions on the theme of the Akathist of the Mother of God. The figures in the frescoes, such as "The Feast of Herod," "The Flight into Egypt," and "The Beheading of St. John the Baptist," are so dynamic that art historian Igor Grabar noted that they "do not stand still, but move, do not walk, but run, leap, and tumble."

The frescoes were restored in 1856 and 1859, using intense shades of blue and gold, which are not characteristic of the original painting. In the mid-20th century, a comprehensive restoration was carried out under the guidance of artist Nikolai Pertsev.