The first church in Sudislavl, an ancient city mentioned in chronicles since the late 14th century, was wooden. In 1758, parishioners built a stone temple with a separate bell tower in its place. The temple had three altars: the main one in honor of the Transfiguration of the Lord and two side altars in honor of the Nativity of Christ and Saint Nicholas the Wonderworker. Documents from 1789 mention another stone Nicholas church near the Transfiguration temple, which was likely dismantled in the early 20th century due to its dilapidation. Its image has been preserved in B.M. Kustodiev's study "Twilight in Sudislavl," which is kept in the Kostroma State Historical-Architectural and Art Museum-Reserve.

A significant event for the Transfiguration temple was the visit on May 15, 1837, by Tsarevich Alexander Nikolaevich, the future Emperor Alexander II, and his tutor, poet V.A. Zhukovsky, during their journey across Russia. In 1898, under the leadership of the archpriest Ioann Dobrokhotov, a new iconostasis was installed by the blessing of Bishop Vissarion of Kostroma and Galich, funded by the parish. The restoration of ancient icons and the correction of wall paintings were carried out with the funds of the temple benefactor Ivan Alexandrovich Kokarev, who donated 3000 rubles.

In the early 20th century, the clergy of the temple consisted of two priests, a deacon, and psalmists, with 1500 parishioners. Among the temple's relics, ancient icons of the Great Martyr Paraskeva Friday, Saint Nicholas the Wonderworker, the icon of the Mother of God "Joy of All Who Sorrow," the icon "The Mourning of the Most Holy Theotokos," and an ancient carved cross with relics of saints were especially venerated. The cemetery church of the Assumption, built in 1790, was attached to the temple.

From 1922 to 1928, the temple was led by the priest-martyr Vasily Razumov, who was shot in 1937 for his faith. At the end of 1928, the temple was closed, but services resumed in 1945 after the Great Patriotic War. Today, the Transfiguration temple is the spiritual center of the Sudislavl district and one of the main attractions of the city. Since 1971, the archpriest Ioann Chernoguz has served as the rector. Repair and restoration work was carried out in the temple for its 250th anniversary, which now amounts to 255 years.