Originally erected between 1158 and 1160, the cathedral, with six pillars and five domes, was expanded from 1185 to 1189 to reflect the augmented prestige of Vladimir.

At 1,178 square metres (12,680 sq ft), it remained the largest Russian church for several hundred years.

Andrew the Pious, Vsevolod the Big Nest (r. 1176–1212) and other rulers of Vladimir-Suzdal were interred in the crypt of this church.

Unlike many other churches, the cathedral survived to some extent the great devastation and fire of Vladimir in 1238, when the Mongol hordes of Batu Khan captured the city.

A lofty belltower, combining genuine Russian, Gothic and Neoclassical influences, was erected nearby in 1810.