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This cathedral, built in 1505-08 by Alevis Novi, was the burial church of the czars. Here all the Russian princes, grandprinces and tsars from Ivan Kalita onwards had their last resting-place (with the exception of Boris Godunov, who, with his wife, are buried in the Monastery of the Trinity at Sergiev Posad). The present church was built on the foundation of an earlier church built by Ivan Kalita in 1333 in thanks giving for relief from famine.
The original church had frescoes (not preserved) painted by Feofan Grek (Theophanes Greek) in 1399. The demolition of the first Cathedral of the Archangel began on 21 May 1505; the new one built by Alevisio the Younger, a rectangular structure with a system of five domes offset towards the east end, was consecrated on 8 November 1508. The two slightly smaller domes are over the lateral apses. Unlike the other Kremlin cathedrals, the Cathedral of the Archangel has silver domes, apart from the recently gilded central dome.

The cathedral was surrounded on three sides by galleries; these were demolished in the 18th century with the exception of part of the south gallery. The tent-roofed annex at the south-west corner was built in 1826, and the buttresses on the south side were also later additions.
The cathedral was thoroughly restored in 1955. Though built at the beginning of the 16th century, the Archangel Cathedral was painted only in the second half of that century. Only part of this painting has survived - in the altar and on the west portal. In 1652-66, a large team of artists from Yaroslavl, Kostroma, and Vologda under direction of Simon Ushakov and Stepan Riazanets painted the cathedral's frescoes, repeating the motifs of the sixteenth century painting.