The first wooden church, built in 1562, was destroyed by fire in 1680. In 1681, with the blessing of Patriarch Joakim, the construction of a new temple began. Since the new temple was significantly larger, the site used for its construction was where the wooden Church in honor of Nicholas the Wonderworker had previously stood, which also burned down in the fire of 1680. The construction was completed in 1687, and on December 21 of the same year, the temple was consecrated by Archimandrite Theodosius from the Ipatiev Monastery.

In the 18th century, the temple was rebuilt, and two new chapels were added: one in honor of Nicholas the Wonderworker and the other in honor of the Theodorov Icon of the Mother of God. A stone fence around the church cemetery with three gates was completed by 1811.

In the early 20th century, the temple was rebuilt again: two old chapels were dismantled, and in their place, a new warm refectory with two new chapels was constructed. The work was overseen by engineer I. V. Bryukhanov and was completed in 1903.

Worship continued until 1949, after which the temple was closed and restoration began, carried out by the Kostroma Special Scientific Restoration Workshop. The work was completed in 1960, and an exhibition of the Kostroma Historical and Architectural Museum was placed in the temple. In the 1970s, architect K. G. Torop conducted restoration of the fence with gates. Later, when the museum occupied the entire territory of the Ipatiev Monastery, the temple housed the monastery community. In 2005, the temple was fully transferred to the diocese.

The temple is adorned with five domes. To the west, it is adjoined by a refectory, which is connected to a tent-shaped bell tower. The temple resembles the Trinity Cathedral of the Ipatiev Monastery located nearby. For example, its slightly flattened domes are similar to the cathedral's. The main attraction of the Church of John the Theologian is the frescoes that cover the entire interior space. They were created by the residents of the Ipatiev sloboda, and the names of the artists are indicated on a plaque preserved on the northern wall of the temple.