There are different opinions regarding the construction date of the Chrysostom (Myrrhbearers) church. Some researchers date it to the early 18th century, while others suggest that the temple could have been built in the 16th century. Clerical records indicate the 17th century, but the exact year of construction is not specified.

This unique church is located at the intersection of the VI Army Embankment and Engels Street, which were previously called Chrysostom streets due to the temple.

Architecturally, the Church of John Chrysostom has direct analogues in monastic construction; for example, there is a similar church in the Spaso-Prilutsky Monastery, the warm church of the Entry into the Temple of the Most Holy Theotokos, dating back to the second half of the 16th and 17th centuries.

The two-story Chrysostom church, in its volumetric solution, resembles the Church of Constantine and Helena: a two-light cube on a basement with five large domes, lowered rectangular extensions, an altar, and a porch, as well as a bell tower at the northwestern corner. The bell tower is the most successful and typical part of the temple. A powerful square base supports a narrow octagonal bell chamber, covered with a pyramidal stone roof with two rows of sound windows and topped with a dome. The character of the masonry and decorations confirms that the bell tower was built before the 18th century.

The church is one of the first two-story temples in Vologda. It consists of two spaces: the lower and upper churches. This reflects the idea of continuity of double Vologda churches, combining cold and warm churches in one building. The altar of the upper church is consecrated in the name of John Chrysostom, while the lower one is in the name of the Myrrhbearers.

In the early 20th century, the Chrysostom church was abolished, and during the Soviet era, it was closed.

In the early 2000s, the church was returned to the faithful and became a subsidiary of the Church of the Intercession on Torg.

In 2010, reconstruction work on the temple began under the supervision of the Department of Culture and Protection of Cultural Heritage Sites of the Vologda Region.

According to the decree of June 25, 2014, Bishop Ignatius of Vologda and Veliky Ustyug established the parish of the Church of St. John Chrysostom in Vologda of the Vologda Diocese of the Russian Orthodox Church, Moscow Patriarchate. Priest Alexey Kalin was appointed as the rector of the church.