The church is located in the former episcopal village of Gorodishche. According to B. L. Altshuller’s research, the temple was built in the second half of the 14th century, while more modern data from S. V. Zagraevsky suggests it was constructed in the early 14th century. The structure was erected from roughly hewn white stone blocks. To this day, the walls of the square base have survived to about half their height, along with the walls of the apses. In the 16th century, the church was significantly rebuilt: the upper part of the building was reconstructed from brick and smoothly hewn white stone, and the facades were divided into three sections by pilasters. In 1780, a new bell tower and refectory connected to it were built. After numerous alterations, the church acquired three altars: the main one in honor of the Conception of John the Baptist, and two in the refectory, in honor of Saint Nicholas and the Apostle James, the Lord's brother. In 1965 and 1969, the church was restored under the guidance of M. B. Chernyshev, which returned it to its presumed appearance of the 16th century.

Initially, the temple had one dome with corner pilasters supporting the arches. After the upper part was rebuilt and a cross vault was erected, the building became a column-free parish church, characteristic of Moscow architecture of the 16th century. The building is now adorned with three drums and a bell tower. The central drum is light, while the side drums are blind. The bell tower has a square base, an octagonal belfry, and a tent roof with openings. The refectory consists of three parts with cross vaults. Near the northern entrance to the church, a carved white stone block is embedded in the wall with mortar from the 14th century. According to N. N. Voronin, it depicts a unicorn, while S. V. Zagraevsky believes it shows a basilisk. The carving on this block resembles the style of Vladimir architects from the 12th century. The original block is currently stored in the Kolomna Local History Museum, while a plaster copy is installed on the church.

Before the revolution, the church housed a Gospel from 1661. The ancient iconostasis was of particular value. Only one icon from the 14th century has survived, "John the Baptist, Angel of the Wilderness," which is kept in the reserves of the Tretyakov Gallery.