The earliest mention of the church dates back to 1679, when the "warm church of the Beheading of Saint John the Baptist with the chapel of Saint Paraskeva the Great Martyr" was noted in the census books next to the Annunciation Cathedral. At that time, it was still a wooden structure. It is believed that the stone church was built with the funds of merchant Ivan Shiryayev from Gorokhovets. Due to its architectural features, masonry technique, and facade decor, the Church of John the Baptist is similar to the Church of John Climacus in the Nikolsky Monastery of Gorokhovets, allowing us to date its construction to the first quarter of the 18th century.

The Church of John the Baptist is part of the ensemble of the Annunciation Monastery. It is located to the north between the bell tower and the Annunciation Cathedral, with its southeast corner almost touching the cathedral. The church completes the monastery's territory on the northern side. It is a low, elongated warm church consisting of a refectory and an apse.

The temple is an element of the monastery complex. It is a low elongated church, typical for warm churches, with a three-part volumetric-compositional structure. It has some common decorative elements with the main monastery church, the Annunciation Cathedral, such as round kokoshniks and drum decor. The volume of the apse is also executed in a similar style.