In the 16th and 17th centuries, a women's monastery was located on the site of the current church. In 1750, construction began on a large stone church on the left bank of the Vologda River, replacing a wooden one of the same name. The church was originally intended for two wealthy monastic villages, Vypryagovo and Korovnichye. Construction continued until the mid-19th century. A tall two-light cold church was added to the eastern side of the church, consecrated in 1755.

In the 1930s, the church was closed, looted, and fell into disrepair. The icon "Miracle of Flora and Lavra" from the second half of the 16th century was transferred to the Vologda Museum-Reserve. Later, the building was used as a warehouse.

There were rumors of sectarians conducting various rituals on the church grounds. In the late 20th century, a private individual attempted to start restoration, which caused discontent among the abbot of the Spaso-Prilutsky Monastery. Only decades later was a blessing received for restoration, but the work was limited to measurements and the creation of a sketch project. An initiative group repeatedly organized clean-up days, removing trash and cutting down trees that had grown on the walls and roof. The building remained unattended, lost many architectural elements, and part of the roof of the refectory collapsed.

Today, St. Nicholas Church is in an emergency state. The roof is almost non-existent, and the vaults and walls are deteriorating due to moisture. The monks of the Spaso-Prilutsky Monastery, to which the church now belongs, have installed temporary windows and doors and restricted access to outsiders. In 2016, a fundraising campaign for restoration was organized.