This church is the oldest in Poltava. In the middle of the seventeenth century it was probably a side precinct of the wooden Church of the Transfiguration of Christ, which burned down in 1705.

It is known from old church chronicles that before 1709 a local priest, Ivan Svitaylo, had bought an old wooden church of the Transfiguration of Christ from the Poltava Monastery of the Exaltation of the Holy Cross to replace the burnt church. According to folklore, following the Battle of Poltava, a Moleben was celebrated where Peter the First was present, while on the church grounds, the fortress defenders were buried. In 1810-1811, when the church had fallen into decay, the decision was taken partly to demolish it. Only one single-cupola side precinct was left as a reminder of its outstanding role in the history of the Russian Empire. In 1837, Oleksandr II visited Poltava. From the funds granted for the upkeep of monuments and those, which were gathered through subscription, in 1845 following the plans of Kharkiv architect A. Ton, a brick exterior was raised over the wooden church, creating the impression of a single domed church. In 1847, in front of the western entrance, a brick bell tower was constructed. From 1875 to 1898 it was used as a regimental church for the 33rd infantry regiment, then deployed in Poltava. In 1890, a brick and iron fence was placed on the boundary of the church yard.

In 1902 a decision to make a thorough restoration of the church was taken by the Most Holy Synod of the Orthodox Chutch. Its fate has been fortunate, as it was not blown up or razed to the ground by bulldozers (like many other city churches) during the Stalin era. Before the revolution of 1917 there were about 20 churches in Poltava.The Church of the Savior is one of the three local churches that survived the terrible 1930s, when many religious buildings were destroyed on the orders of Jozef Stalin. The bell tower was blown up in 1934. After 1942 the church renewed its activity as a parish of the Moscow patriarchy.