Father Innocent Veniaminov designed the cathedral in the Russian church style. The Russian-American Company paid for it, and it was finished on November 20, 1848. The bells were forged in Alaska, and the clock in the bell tower was made by Innocent.
In 1867 Alaska was sold to the United States, and soldiers who arrived with Major General Jefferson C. Davis pillaged the cathedral. It stood for more than a hundred years until a fire destroyed it on the night of January 2, 1966. The royal doors and a chandelier were saved, but the bells, the clock and a library of books in Russian, Tlingit and Aleut were lost.
The new cathedral is a copy built to the same measurements at the same spot, from 1961 survey drawings. It is made of concrete and steel with vinyl siding, and it was re-consecrated in 1978.