Unlike most ancient Novgorod churches, this one was built during the era of Moscow Rus, in 1557. This date is mentioned in all publications as the year of the original construction. At that time, the area had a less organized layout than it does now; the Great Moscow Street did not yet exist, and the church faced the now-disappeared Nikitina Street.

However, it is worth noting that during the period of Novgorod's independence, chronicles mention a church of the same name in this area twice. During the fire of 1368, the right-bank Plotnitsky end of the city suffered from the flames, and among the burned buildings, this church was likely included.

Later, Metropolitan Makary Mirolubov, a specialist in Novgorod church antiquities, claimed that the Church of Nikita was rebuilt in stone in 1375. However, by 1406 it had again fallen into disrepair, and according to the Novgorod I Chronicle, three new churches were built, including the Church of St. Nikita in the Plotnitsky end.

This church served as a street church, as there were no other churches on Nikitina Street. The street assembly gathered in front of it. Novgorod street residents had the right to build churches on their street, manage land, and complain about the arbitrariness of representatives from other areas.

For example, a Hanseatic report describes how the residents of Mikhailov Street, with the involvement of authorities, forced the residents of the German merchant courtyard not to expand their gates. The residents of Nikitina Street also fought for their rights. In 1475, they complained to Grand Duke Ivan III about the arbitrariness of the posadnik from the Nerev end.

Ivan III, who was then at Gorodishche near Novgorod, used this as a pretext for a legal proceeding known as the trial at Gorodishche. This event became a pretext for the final annexation of Novgorod to the Moscow state.

In 1558, the church was rebuilt in a style unique to Novgorod. The architects did not adhere to symmetry: the bell tower was located at the apses, and a chapel dedicated to St. Nicholas the Wonderworker was added diagonally. In the 1570s, Nikitina Street, along with the church, likely found itself on the territory of Tsar Ivan the Terrible's court.

In 1571, after the devastation of Novgorod, the tsar and his sons arrived at the Tsar's court on Nikitina Street. Even after Ivan the Terrible, the church remained one of the most significant in the city. In the 17th century, services were held here by Novgorod archbishops. In 1722, a narthex was added to the church.

In the 1730s and 1780s, the area was redesigned, and the church ended up in the backyards, as Nikitina Street disappeared. It became an ordinary parish church on the northern outskirts of the historical part of the city.

In 1813, the dilapidated vaults of the church were replaced, and it received a low dome on a wide drum. At that time, a spire was also created on the bell tower, and the western narthex was faced in the style of classicism.

During the Soviet era, the church was closed and housed a chess club. In the post-perestroika period, the building fell into disrepair and became a shelter for the homeless. In the 2000s, it was seriously restored, but the basement with the staircase and the interior still need repairs.