The Church of John on Opokah was built between 1127 and 1130 by Prince Vsevolod Mstislavich, who transferred it to the Novgorod merchants known as "Ivanovsky St" through a special charter. A merchant court operated at the church, headed by the Tytsytsky, which dealt with the resolution of trade disputes. The church also served as a kind of chamber of measures and weights.

It housed standards such as the "Ivanov elbow" for measuring the length of cloth, the "grivenka ruble" for weighing precious metals, "waxed scales," weights, and other samples.

The existing church dates back to 1453, when the original was dismantled, and by the order of Archbishop Euthymius, a new one was built on the old foundation using part of the walls, preserving the previous architectural style.

The architecture of the Church of John on Opokah represents a transitional stage in the history of Novgorod architecture. On one hand, it retains the traditions of grand princely construction from the early 12th century, while on the other hand, there is a trend towards reducing volume and simplifying architectural forms. The temple has a six-column structure with three apses and a gable roof over each semicircle, decorating the facades. The pilasters on the facade correspond to the internal divisions. The smooth walls with narrow windows give the building a strict simplicity. The structure is topped with a single dome, although there were more in the past.

In 1934, the church bell tower was demolished. During World War II, the church suffered greatly, completely losing its drum, dome, and roof, and sustaining breaches in the walls and northern apse. It was restored in the mid-1950s.