Before the cathedral was built, services for Tolyatti's Auto Factory District were held in an ordinary flat in a conventional 16–storey apartment building on Yubileynaya (Jubilee) Street.
In August 1991 (at the same time as the 1991 Soviet coup d'état attempt was unfolding), the Tolyatti town planning council made the decision to build a temple complex consisting of a baptismal church, a bell tower, and the Transfiguration Cathedral.
The original intent was to place the cathedral on the banks of the Volga, but it was later decided to build it closer to the residential areas.
For the opening of the cathedral, Tolyatti jewelers provided sixteen enamel icons in silver frames.
In July 2006, the cathedral hosted one of the most important relics in the Christian world, the supposed right hand of John the Baptist.