The Church of John the Theologian in Cherdyn, built in 1718, is the oldest structure in the city. It is located at the edge of a deep ravine, on a riverbank slope that steeply descends into the river valley. Previously, there was a monastery of John the Theologian, founded in 1580 and granted privileges by Ivan the Terrible, making it the oldest monastery in the Ural region. In 1631, the monastery was attached to the Trinity-Sergius Lavra near Moscow. A fire in 1700 destroyed two wooden churches of the monastery.

In their place, a stone church was built, surrounded by an iron fence with brick pillars and three-bay gates. Permission for its construction was granted by Archbishop Dionysius in March 1717 to the abbot Grigory. According to the decree, the church was to be built of stone and brick using lime and timber, have one, three, or five domes, a round and bright altar, and comply with established rules and regulations. The construction was overseen by Lev Kolotilov, while Ivan Vetoshev monitored the work. The client was the Siberian governor Matvey Petrovich Gagarin, who had previously passed through the city. He also sent captured Swedes, exiled to the Kama region by Peter I after the Battle of Poltava in 1709, to assist with the construction.

The Church of John the Theologian is small, made of brick, with a four-pitched iron roof. It consists of an elongated square base, with a winter church in the lower part and a two-light summer church above. To the east, a high semi-cylindrical apse adjoins the square base, and to the west, there is a refectory with a lower narthex. Originally, the church was surrounded by a vaulted gallery, dismantled in the late 18th and early 19th centuries.

The decorative finishing of the church is quite simple. The corners of the building are adorned with subtly expressed rustication. Large rectangular windows stand out against the whitewashed walls. In the lower part of the square base, the windows have frames with raised rounded tops, replacing pediments, while in the upper part, they are outlined with frames without semicircles. The frames of the lower windows of the apse and the light openings in the upper part of the square base, where doors to the gallery once were, feature baroque decoration.

The cornices of the building have a slight overhang and are made of brickwork with a frequent band of small bricks. Above the cornices of the refectory and apse rise small blind attics, likely of later origin, repeating the attic of the square base with semicircles imitating arches.

Of particular interest is the octagonal bell tower of the church, located on the vault of the square base. It distinguishes the church among other architectural monuments in the region. Its placement above the roof brings the composition closer to Moscow's multi-tiered churches of the late 17th century. In the past, specially cast bells hung between the arched openings of the bell tower, adorned with balusters. The onion dome of the church, visible from any part of Cherdyn, crowns the faceted drum on the bell tower's vault.