The Church of St. Demetrius of Thessalonica was founded by the Moldavian ruler Dmitry Cantemir, who also established the city of Dmitrovsk, in 1721. However, the completion of the construction and the consecration of the church took place only in 1725.

Initially, the church was dedicated to Saints Demetrius of Thessalonica, Emperor Constantine, and his mother Helena. It was the first church in Dmitrovsk, serving as the household church of the Cantemir princes, and remained the only one until 1787. In 1789, the church was rebuilt, but the iconostasis and icons were preserved in their original form. The church has two altars. In 1802, it received the status of a city or Cathedral church. Today, it is the only surviving and functioning church in Dmitrovsk.

By the end of the 19th century, the city had 8 churches and three chapels, including the Kazan Church (since 1787), the Trinity Cathedral (since 1812), the Church of John the Baptist at the cemetery (since 1842), the Protection Church (since 1863), the Sumeonov Church at the prison castle (since 1873), an Old Believer church, as well as chapels in honor of the icon of the Mother of God "Joy of All Who Sorrow," with the icon of St. Nicholas the Wonderworker and the icon of St. Blaise. After the construction of the Trinity Cathedral in 1787, the Church of St. Demetrius of Thessalonica became a parish church, but the townspeople still call it the "Old Cathedral." On the feast day of the church, June 4 (May 22 in the old style), a fair called "Tsari" was held, which was the oldest in Dmitrovsk and began in the late 1720s. This fair remained the only one until the appearance of other churches and fairs, and later became the largest and most vibrant. After the city was liberated from the fascists in 1944, the destroyed church was restored by the photographer-artist A.A. Teterkin, the son of the well-known church painter A.A. Teterkin, who arrived in Dmitrovsk from Karachev in 1891.

Today, the Dmitrov Church is located in the southern part of the city, not far from the center, at 25 Socialist Street.