The first warm church of the Dmitrievsky parish was built in 1710-1711 near the northern wall of the Church of Dmitry Prilutsky on Navolok. It was consecrated in honor of Saint Prince Feodor and his sons David and Konstantin, the Yaroslavl miracle workers, which confirms the involvement of Yaroslavl masters in the construction of the cold Dmitrievsky church. Presumably, a bell tower was also erected in the 18th century. In 1750, the chapel of the Yaroslavl miracle workers was dismantled, and with the funds of merchant A. A. Rybnnikov, a separate warm church was built. According to some sources, it was originally called All Saints, and in 1836 it was re-consecrated as the Assumption Church on Navolok.

The warm church, consecrated in honor of the Assumption, is a low rectangular building, elongated in length, characteristic of northern winter churches. It has preserved its original appearance with a two-tiered dome and two apses formed by the altars of the main church and the chapel. The facade decor includes simple pilasters and cornices with teeth. On the western side, a baroque bell tower adjoins the church, featuring a square base, two octagonal sections, and a dome. The decor consists of paired flat pilasters, toothed cornices, and window frames with eyebrows, typical of the first third of the 18th century. The prospective portal and large lintels under the ringing arches resemble older examples of ancient Russian architecture.

The churches of Dmitry Prilutsky and the Assumption of the Mother of God were closed from March 6 to 13, 1930. From May to July of the same year, representatives of the Dmitrievsky community appealed to the provincial and district administrative departments requesting the return of the churches, indicating the temporary nature of the closure. However, a special commission, which included representatives of the city council, the OGPU, and other agencies, rejected the petition, noting that "the churches were closed at the request of the believers themselves and the majority of working organizations."

On April 6, 1930, at a meeting of the secretariat of the Vologda city council, a decision was made to dismantle the church fences and churches that were unsuitable for cultural purposes. The commission, consisting of representatives from various organizations, deemed it possible to demolish the warm Assumption church as well. Fortunately, this plan was not realized.

In the 1930s, the closed Dmitrievsky churches were transferred to the military department, and part of the church property was sent to the Vologda Local History Museum.

By the decree of the Council of Ministers of the RSFSR on August 30, 1960, the Ensemble of Dmitrievsky Churches, including the Church of Dmitry Prilutsky and the warm Church of the Assumption, was recognized as a cultural heritage site of federal significance. In the 1980s, restoration work was carried out.

In the late 1990s, the Assumption Church and then the Dmitrievsky Church were returned to the believers. Currently, the churches are part of the Spaso-Prilutsky Monastery.