The Nativity Cathedral was the main Orthodox church of Murom, towering on Voievodskaya Hill above the Oka River.

In 1458, the cathedral was restored through the efforts of Ivan III of Moscow. In the 16th century, the first Russian tsar, Ivan the Terrible, prayed here multiple times. In 1552, after the capture of Kazan, he allocated funds for the construction of four stone churches in Murom, including the city cathedral. The church was built on a high foundation that served as an arsenal for storing weapons.

According to the land survey book of Bartenev from 1636/37, the city had the cathedral church of the Nativity of the Most Holy Theotokos with three domes and a stone porch. In the chapel of the supreme apostles Peter and Paul rested the relics of the Murom miracle workers, the righteous prince Peter and princess Fevronia, covered with black cloth, and above the reliquary was their image. The construction of this cathedral church was the merit of Tsar Ivan Vasilyevich.

In the 19th century, archpriest Leonid Belotsvetov described the church as very magnificent. Four massive pillars supported its vaults, light penetrated through 19 windows arranged in two rows, and 39 windows in five domes. Under the central dome hung a massive chandelier made of silvered copper with 40 candles, and on the sides, two smaller chandeliers with 36 candles. The eastern wall was occupied by a five-tiered gilded iconostasis with 62 icons, decorated with columns featuring fine carvings.

After the revolution, the cathedral was subjected to looting and desecration; some ancient icons and church utensils were transferred to the local museum, as were the relics of Peter and Fevronia. In 1924, the cathedral was closed, and ten years later it was handed over to the military. A football field was set up in front of the church, and the bell tower was used as a changing room for athletes. In 1939, the dismantling of the 400-year-old walls of the church began. The bell tower stood longer, as it served as a fire watchtower. Now, on the site of the cathedral complex, there is Lenin Park ('Oksky').