In this place, the first wooden church was built in the 17th century, which fell into disrepair by the early 18th century. In 1722, Moldavian prince Dmitry Cantemir, the owner of the estate Black Mud, erected a new temple with a stone foundation and a wooden upper part, crowned with a single dome. In 1759, Prince Matvey Cantemir the Younger received permission from the Moscow metropolitan to dismantle the old church and build a new, entirely stone one. The new temple was made of brick in the Elizabethan Baroque style, with a white stone base and decor. A two-tiered bell tower adjoins it from the west. The consecration took place on June 23, 1765.

In 1775, Catherine II acquired the estate and renamed it Tsaritsyno. Under the guidance of architect Vasily Bazhenov, the construction of the imperial residence began, which included the temple.

During the War of 1812, the church was damaged. In 1813, the overseer of Tsaritsyno, A. Egorov, reported that in September 1812, enemy troops damaged the church doors and looted some items.

By the end of the 1880s, Tsaritsyno became a prestigious dacha settlement. The temple and bell tower were reconstructed according to the project of the bureau 'P. N. Lavin and Co.' The refectory was expanded, and the southern chapel was consecrated. Inside, the church was decorated with paintings and stucco. The floor was made of asphalt with marble chips.

The bell tower became four-tiered with six bells, the largest of which weighs 180 poods.

After the October Revolution of 1917, the church continued to operate despite the anti-clerical activities of the 'Political-Sports Union of Youth.' In the 1920s and 1930s, representatives of noble families, such as the Obolenskys and Sheremetevs, visited the church. Services and sacraments continued.

However, in 1934, the bells were removed, and in 1938, the church was closed. Some icons were taken by parishioners and clergy, some were transferred to museums, but most of the church utensils and icons were destroyed.

From the 1940s, the church building was used as a transformer substation, and in the 1970s, as a printing house. In 1975, a woodworking workshop of 'Soyuzrestavratsiya' was located here.

In the autumn of 1990, the church was handed over to the community of believers, and services resumed. The paintings from the late 19th and early 20th centuries and Baroque stucco from the 18th and 19th centuries have been preserved.

On May 6, 1998, the church was consecrated again by Patriarch Alexy II.