The original wooden church, dedicated to Dmitry of Prilutsk, was known as the Church of Dmitry of Prilutsk on Kobyliya Street in the 17th century. It is believed to have been built in 1503 on the site where the tomb icon of Dmitry of Prilutsk was located, returned from Ivan III's victorious campaign against the Tatars. In the 16th century, this was the starting point for the road to Kostroma and Moscow, where a meeting could have taken place. According to another version, during Ivan the Terrible's campaign against Kazan, the life icon of Dmitry of Prilutsk was taken from the Spassky Cathedral of the Prilutsk Monastery. Around 1690, a stone church was built on the site of the wooden one, which has survived to this day. It is suggested that this church is mentioned in connection with the construction by Yaroslavl masters of the Church of Dmitry of Prilutsk in Vologda in 1653, rather than the church on Navolok. The church is consecrated in honor of the holy equal-to-the-apostles kings Constantine and Helena, while the chapel of the lower church is dedicated to Dmitry of Prilutsk. In memory of the event that served as the foundation of the church, a liturgy was held annually on June 3 in the Cathedral and the Church of Constantine and Helena, followed by a procession to the Spaso-Prilutsky Monastery.

Until the early 20th century, the church was located on the outskirts of the city. It was closed on February 24, 1930, and cultural institutions and a knitwear factory were placed within its walls. The interior of the church was destroyed and looted, and it housed a storage facility for a household store. In 1997, the church was returned to the Russian Orthodox Church, and restoration began. In 1998, regular services resumed in the lower church, and since 2008, in the upper church as well. The tradition of processions was revived. On April 10, 2008, eight new bells weighing from 10 to 430 kg were raised to the bell tower, delivered from Tutayev.

The tented bell tower, adjoining the porch from the north-west side, was built simultaneously with the main building of the church. It consists of three tiers in the form of octagons of the same diameter, reaching down to the ground, following ancient traditions. The upper octagon is open for ringing, formed by arches with keel-shaped finishes and decorated with triple half-columns. The bell tower is topped with a light tent with sound windows and a small dome.