The Cathedral of the Nativity of the Blessed Virgin Mary in Vladimir, which is the main church of the Nativity Monastery, is located in the eastern part of its territory. The cathedral was originally built between 1192 and 1196 at the initiative of Prince Vsevolod III of the Big Nest. It was a four-pillar, three-apsidal, single-domed church, executed in the style of Vladimir-Suzdal architecture of the late 12th century. The great consecration took place in 1219. The history of the cathedral and the monastery is closely linked to Prince Alexander Nevsky, under whom the monastery became the main abode of Northeastern Rus until the 15th century. In 1263, Prince Alexander Nevsky was buried here, and his relics remained in the cathedral until the 18th century, when in 1724, by order of Peter I, they were transferred to St. Petersburg, to the Alexander Nevsky Lavra. Between 1678 and 1685, under Archimandrite Vikentiy, stone chambers were added to the cathedral, which have not survived. From 1858 to 1868, the heavily reconstructed and dilapidated cathedral was dismantled and rebuilt according to the design of architect N.A. Artleben, but without galleries and using white stone and brick. The new church resembled the Dmitrievsky monastery, differing in its strict exterior design. The facades are adorned with ornaments, lions, and female masks, with patterns carved from smoothly hewn stone. The monastery created the Laurentian Chronicle and also wrote the Life of Saint Prince Alexander Nevsky. Today, the main relic of the monastery is the relics of St. Athanasius, Bishop of Kovrov. In July 1930, the cathedral was dismantled, and a sports ground was arranged in its place.

In 1992, the monastery was returned to the Vladimir-Suzdal Diocese, and it began to operate again. Later, a wooden chapel was erected on the site of the lost cathedral. In September 1995, Patriarch Alexy II of Moscow and All Russia consecrated the cornerstone of the new cathedral in honor of the Nativity of the Blessed Virgin Mary. Before the restoration of the church from 1995 to 1999, archaeological excavations were conducted, during which many details of the 12th-century cathedral were found, and the foundation was fully uncovered. In 1999, the construction of the new cathedral began, which became a memorial church. The work was carried out by the diocesan administration in collaboration with the administration of the Vladimir region. The consecration of the new cathedral took place on August 21, 2004, by Metropolitan Kliment Kapalin and Archbishop Evlogy.

The goal of the new cathedral's construction was not to reproduce the appearance of the ancient church. As explained by Igor Stoletov, director of OAO 'Vladimirrestavratsiya', the architecture of the new church represents a synthesis of white-stone architecture of the 12th century, created in the 21st century. The only direct restoration was the placement of the cross of the new cathedral exactly in line with the vertical of the cross of the previous church. The new Cathedral of the Nativity of the Blessed Virgin Mary in Vladimir opened its doors in 2004.