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The first and foremost church in the city of Odessa, the original small building had been built in 1221 during Grand Prince Yurii Ysevolodovich. This had just a single cupola and a tiled roof.

The cathedral was designated the main church of New Russia in 1808 and was continuously expanded throughout the 19th century. The belltower was built between 1825 and 1837, and the refectory connecting it to the main church several years later. The interior was lined with polychrome marble, and the icon screen also was of marble.

Several churches in the region, including the Nativity Cathedral in Chişinău, were built in conscious imitation of the Odessa church. The cathedral was the burial place of the bishops of Tauride (including Saint Innocent of Kherson) and Prince Mikhail Semyonovich Vorontsov, the famous governor of New Russia.

The original structure was demolished by the Soviets in 1936. It was rebuilt starting from 1999. The new cathedral was consecrated in 2003. The remains of Vorontsov and his wife were subsequently reburied in the cathedral. There is a statue of him on the cathedral square. The cathedral bells are controlled by an electronic device capable of playing 99 melodies.

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