The decision to build a winter cathedral was made in the early 1750s under Bishop Serapion. The first attempt to erect the cathedral took place in 1757 under Joseph the Golden, and it was consecrated in honor of the Meeting of the Lord. However, the completed building was dismantled in 1771 due to discovered cracks in the arches, and the cathedral was deemed unreliable for further construction.

The new Resurrection Cathedral was built on the site of the southeastern tower of the Vologda Kremlin. Stones from the destroyed fortress walls and towers were used for construction. It is believed that the cathedral was designed by local architect Zlatitsky based on a model created by a master from the capital. A wooden model with a higher dome and fine details is kept in the Vologda State Museum-Reserve. Construction was completed in 1776, after the death of Joseph the Golden, under Bishop Irinei.

In June 2015, Governor Oleg Kuvshinnikov announced that the cathedral would be transferred to the Vologda Diocese by July 1, 2016. Since December 4, 2016, the cathedral has once again become an active cathedral of the Vologda Diocese.

The Resurrection Cathedral is a two-story oval building with five domes. It includes a refectory, four semicircular chapels on the sides, and an elongated altar. The large dome with oval windows and lanterns is topped with a cupola and surrounded by two-tiered octagonal towers and chapels.

The facades are decorated with Tuscan columns and pilasters, and the windows are framed with ornate surrounds. The main entrance from the Kremlin Square is designed in the Empire style with a pediment and columns of the Tuscan order, prepared for the arrival of Emperor Alexander I. Art historians believe that the original design was simplified and coarsened during construction.

It is difficult to judge the original interior decoration of the cathedral. In 1832 and 1833, the interior was updated. According to G. K. Lukomsky, "inside, the cathedral represents nothing interesting. The painting and ornamentation reflect the poor taste of the Alexander II and III eras, and the icon cases, iconostases, and other items look tasteless, with a craftsman-like coldness and a striving for luxury."

From 1847 to 1928, the refectory of the cathedral housed the 14th-century icon of the Trinity "Zyryanskaya," unique for its inscriptions in the Komi-Zyryan language, made in ancient Permic script.