Originally, the church was located in a utility room on the property of the Bek-Mamedov family. Later, a plot was purchased for $1,000 on 15th South Avenue, where a new church was built in the early 1950s with the active support of I. A. Sitchenko. Following this, Sitchenko and Mazurenko took on the construction of the church house and refectory. In 1962, the church facade was updated and two domes were installed.

In the 1950s and 1970s, St. Petersburg in Florida became a spiritual and cultural center for the first wave of Russian emigration. Since the 1970s, the parish began to be replenished with immigrants from the second wave, mainly due to the relocation of retirees from northern states in the USA and Canada, which contributed to its rapid growth. In 1980, with the assistance of the parishioner A. K. Dremov, another house was purchased for the priest and his family. In the mid-1980s, a fire occurred in the church, causing significant damage. This event sparked discussions about building a new church, but due to a lack of funds and resources, it was decided to restore the old one. In 1996, the old priest's house was sold, and a new one was purchased.

In 1998, the community celebrated its 50th anniversary, which was an important event for all of St. Petersburg in Florida, where the Russian community holds a special place in the city's history. Since the late 1990s, the parish has significantly rejuvenated thanks to new Russian immigrants. As a result, the parishioners had the opportunity to build a new church in a good location. In 2008, the construction of the new church began, funded by parishioner A. V. Alexandrov, a businessman from Russia.

By Christmas in January 2010, the new church was ready, and the altar was moved from the old building. On September 1 of the same year, Metropolitan Hilarion, the head of the Russian Orthodox Church Outside Russia, performed the great consecration of the new church.