After the destruction of Ryazan along with its stone churches, the grand princely court was moved to Pereyaslavl. Soon, the archbishop's court relocated to the nearby city of Borisov-Glebov. At that time, all buildings in Pereyaslavl were wooden, so Grand Prince Oleg of Ryazan began the construction of the first stone cathedral. With the acquisition of cathedral status, each new archbishop sought to improve the cathedral and add something new to its architecture. The Nativity Cathedral has been rebuilt multiple times and has reached our days in the style of classicism, which formed in the early 19th century thanks to architect Stefenhagen. The interior decoration of the cathedral was richly adorned, including a magnificent carved iconostasis. In 1873 and 1875, the walls and vaults were painted by the famous Ryazan icon painter N. V. Shumov, who initiated the completion of the church with an octagonal rotunda with windows, 'an eight on a square.' In the 14th and 15th centuries, five Ryazan princes and three princesses were buried in the cathedral, and in the early 19th century, two Ryazan archbishops. The cathedral was visited by emperors: Alexander I in 1819, 1820, and 1824, Nicholas I in 1832 and 1836, Alexander II, while being the Tsarevich, in 1837, and Nicholas II in 1904 and 1914. The last major renovation of the cathedral before its closure was carried out in 1913, after which the Metlakh tiles remained on the floor. In 1930, the cathedral was closed, and the regional archive was placed in its building. In 2002, the building was returned to the church and consecrated by Patriarch Alexy II.

In 2002, the relics of St. Basil of Ryazan, the first bishop and patron of the Ryazan land, were transferred to the church. Above his burial, one can venerate the reliquary containing a part of his relics. To the right and left of the pulpit are the honorable relics of the Ryazan saints of the 19th century, Gavriil Gorodkov and Meletiy Yakimov. The cathedral also has reliquaries with parts of the relics of many Ryazan saints and 84 venerable fathers of the Kiev-Pechersk Lavra. Additionally, it houses a part of the Lord's Robe, fragments of the relics of the Apostle and Evangelist Matthew, Saints Basil the Great, Gregory the Theologian, John Chrysostom, Venerable Seraphim of Sarov, Blessed Matrona of Moscow, and other holy relics available for veneration.