The first church in honor of the Nativity of the Virgin Mary was built around 1627, replacing the dilapidated Nikolskaya church. At that time, the village was owned by Prince Ivan Ivanovich Shuisky. In 1653, the village became a patriarchal estate and was named Vladikino. On May 19, 1690, Tsar Peter Alexeyevich visited Vladikino and prayed during the liturgy in the local church alongside Patriarch Adrian.

The first stone church was built in 1770, and the bell tower was erected by Count K.G. Razumovsky, the owner of the neighboring village of Petrovskoye.

In 1854 and 1858, the church was completely rebuilt by architect A.F. Yaroshevsky. In 1859, the new three-altar church was consecrated, and the main altar in honor of the Nativity of the Blessed Virgin Mary was consecrated by Metropolitan Filaret (Drozdov).

In his diary on July 31, 1860, Ivan Mikhailovich Snegiryov, a well-known Russian historian and ethnographer, described the consecration of the Church of the Nativity of the Virgin Mary, built by merchant Gavriil Matveyevich Tolokonnikov. The church had five domes with a bell tower, and the consecration was conducted by Metropolitan Filaret accompanied by Archimandrites Ioanniki and Eustathius. Many people attended the event, including the Chief Prosecutor of the Holy Synod, Count Tolstoy. After the consecration, a lavish feast was offered, along with spiritual nourishment in the form of books distributed by Archimandrite Eustathius.

During the Soviet era, the church remained open for services. In the 1970s, it was planned to be demolished for the construction of an overpass on Altufyevskoye Highway, but the parishioners managed to preserve it. In 2013, the first patriarchal service since the post-Soviet period was held in the church, led by Patriarch Kirill.