The Church of John the Theologian, built in 1683, is considered one of the most perfect structures in the Rostov Kremlin. This gate church resembles the Church of the Resurrection: it also stands on a high base and has protruding round towers. However, its main part is elongated upwards, giving the building lightness and elegance, emphasized by the elongated drums. The apses of the church have a slight curvature, which is characteristic of Rostov churches. The western facade and the gates leading to the Moscow road are richly decorated.

The frescoes of the church depict scenes from the life of John the Theologian and Abraham of Rostov, a saint who, according to chronicles, was one of the first preachers of Christianity in Rostov. The lower tier of the paintings is particularly interesting, showing the meeting of Abraham with John and the struggle against idolaters. These frescoes reflect the artist's ideas about ancient Rostov land. In the scene of the meeting on the western wall, Rostov is depicted surrounded by a fortress wall with a tower, nearby is the scene of the destruction of the idol Veles against the backdrop of the city.

A little away from the side tower, on the wall, as with the Church of the Resurrection, there is a small tent-like bell tower reminiscent of the royal turret on the Kremlin wall in Moscow.

The Church of John the Theologian in the Rostov Archiepiscopal House, now known as the Rostov Kremlin, was built in the early 1680s by order of Metropolitan Jonah Sysoevich, a prominent church figure of the 17th century and associate of Patriarch Nikon. The structure above the western ceremonial gates of the Kremlin completed the formation of the Kremlin ensemble. The interior retains wall paintings, the completion of which is noted by an inscription on the eastern wall from 1683. In addition to traditional themes, the wall painting includes life cycles of the Apostle John the Theologian and Saint Abraham of Rostov, one of the first enlighteners of the Rostov land.

The church has one altar dedicated to John the Theologian. It is a five-domed church with one light dome and four decorative domes, featuring a three-part altar and a two-tiered base. It stands above the gates with a bent passage and is surrounded by galleries on three sides, with two round towers located in front of the gates from the city side.

The church burned down twice, and by the end of the 18th century, services ceased, and the cellars were turned into storage rooms. By the early 19th century, the church had fallen into disrepair, and there were plans to dismantle it for bricks to be used in a new church. However, the Rostov city society defended the ancient buildings, but their restoration began only in the second half of the 19th century. By this time, the church had stood without a roof for 30 years, with ruined vaults and broken windows. After the revolution, the church was closed and only shown to visitors of the Kremlin from the outside. A turning point came in 1953 when a strong tornado significantly damaged the building, after which it was thoroughly restored. At that time, the western gates became the main entrance.