The church, located at the beginning of Malaya Dmitrovka, is the last of its kind. Its construction marked the end of an entire architectural era in Russian church architecture. In the 20th century, it remained the only one in Moscow with three tent-like roofs. The construction cost local residents a significant sum.

This part of the street housed the Embassy courtyard with the travel palace, where foreign ambassadors stayed before heading to the Kremlin. Hence the old name of the area, "Putinki." The first wooden church in honor of the Nativity of the Virgin was mentioned in 1625, and there is a version that it already had three tents at that time. In 1648, the church burned down, and a year later, the construction of a new stone building began. Local residents appealed to Tsar Alexei Mikhailovich through the Jerusalem Patriarch Paisius, who was in Moscow, requesting stone and money for construction. The treasury provided materials and 300 rubles. This amount was insufficient, and after a repeated request, an additional 400 rubles were allocated. In 1652, another 100 rubles were added, and in total, the church cost 800 rubles, which was a huge sum for the mid-17th century. However, the church turned out to be unusual.

The architectural feature of the Church of the Nativity of the Virgin in Putinki is the absence of a distinctly expressed main facade: it is richly decorated on all sides and can be viewed from any angle. The structure of the church is also atypical: the square part is elongated from north to south, the bell tower is located in the northeast, next to the three tents of the main part, which are arranged in a row. These tents are not open inside, as in the original tent churches, but are built on top of the vaults and serve a decorative function. The fourth tent crowns the chapel of the Indestructible Bush, built to the north in the form of a separate cube. The bases of all drums and tents are surrounded by kokoshniks.

The church was consecrated in 1652, and already the following year, Patriarch Nikon banned the construction of stone tent churches in Russia, preferring five-domed ones. However, architects were allowed to build tent bell towers until the early 18th century. Thus, the church on Malaya Dmitrovka became the last tent church in Moscow.

In the late 17th century, the refectory with the chapel of St. Theodore the Tyro was expanded from the southwest, receiving a more modest decor. In 1864, for the visit of Emperor Alexander II, a new closed porch was added from the west, decorated with a tent in the style of the main church. In 1911, a tenement house was built from the south, partially blocking the view of the church.

During the Soviet era, other Moscow churches of similar architecture were either destroyed or lost their roofs. The Church of the Nativity of the Virgin in Putinki, despite the cessation of services after 1935, preserved its facades. Only the porch was remodeled in 1957: it became open and resembled the entrance to 17th-century chambers. The interior decoration was destroyed, and for a long time, the church housed a rehearsal base for the Moscow directorate of "Circus on Stage."

In 1990, the church was returned to the faithful, and actor Alexander Abdulov greatly assisted in its restoration. It was here that his funeral took place on January 5, 2008. The church has the status of a patriarchal courtyard.