Since 1630, the White City was surrounded by a stone wall, and before that, it was protected by a wooden palisade made of sharpened logs driven into the ground, known as an ostrog. This ostrog was built in 1559 by clerk Ivan Vyrodkov, who was sent to construct the Astrakhan Kremlin. He also built the first church in the ostrog in honor of the Nativity of the Blessed Virgin Mary, presumably in 1560. Initially, it was wooden and had one altar.

The construction of this church was motivated by special reasons. Tsar Ivan Vasilyevich the Terrible, like many educated people of that time, including Saint Metropolitan Macarius of Moscow, believed that Astrakhan was the ancient Tmutarakan, one of the domains of Russian princes. In 1556, while sending troops to conquer the Astrakhan Khanate, the tsar recalled how his ancestor, Saint Prince Vladimir of Kiev, distributed lands to his children, giving Tmutarakan to his son Mstislav, who built a temple there in honor of the Most Pure Mother of God. In memory of this, the tsar instructed clerk Vyrodkov to build a church in honor of the Nativity of the Blessed Virgin Mary to emphasize the spiritual continuity between ancient Tmutarakan and the new Astrakhan.

Initially, the temple served as the main cathedral of the city until 1568, when Abbot Cyril erected a new cathedral in the Kremlin in honor of the Meeting of the Vladimir Icon of the Mother of God. After that, the Nativity of the Blessed Virgin Mary Church became an ordinary parish church, with parishioners mainly consisting of archers. In the 1630s, mounted archers settled in the White City, and this place became known as the Archer Town or Sloboda. By the end of the 17th century, the church had fallen into disrepair and was completely rebuilt in 1684 by order of Patriarch Joachim, who instructed changes to its architecture.

After the 1917 revolution, the Nativity of the Blessed Virgin Mary Church twice became the cathedral church of Astrakhan. The first time was from January to April 1918, when access to the Kremlin and the Assumption Cathedral was closed after battles. The second time, after the seizure of the cathedral by the Renovationists in 1923, when Archbishop Thaddeus Uspensky made it his cathedral.

In February 1924, the Renovationists seized the lower church, and in April, the upper one. In the 1930s, local authorities took the church from the Renovationists. Although the Nativity of the Blessed Virgin Mary Church was recognized as a monument of architecture, the commission decided to demolish it in 1932, believing that the city had enough of one baroque church, the Assumption Cathedral. In the same year, the church was dismantled. Now, on its site, at the intersection of modern Soviet and Communist streets, there is Pushkin Park.