In 1994, Archbishop Juvenal of Kursk and Rylsk blessed the opening of a new parish in the Industrial District (now the Seymsky District) of the regional center. This area formed in the post-war years on the site of the villages of Ryshkovo and Lomonovo after the construction of a rubber technical products factory and other industrial facilities. The administrative and cultural center of the district concentrated around Rokossovsky Square and Kulakov Avenue. There had never been a church in this area, and residents of the largest district had to travel to the historical center of Kursk. The first significant event of the new parish, led by Priest Leonid Solokhin, was the launch of a daily Orthodox radio program "Znamenie" on one of the city's FM stations, which became a kind of business card for the parish.

The first service took place at the building of evening school No. 12 on Rezinoi Street on the day of the Holy Epiphany in 1997, and the first liturgy was held on February 15 of the same year in the evening school building. On November 17, the project for the construction of the first phase of the new church, developed by architect Viktor Nikolayevich Mikhailov, was approved. In December 1997, the laying of the first piles for the future Baptismal church and Sunday school began. The foundation was consecrated on the day of the Holy Trinity, and the first service took place on August 19, 1998, under the guidance of Archbishop Juvenal of Kursk and Rylsk. From the Feast of the Protection of the Holy Mother of God, services began to be held daily in this building.

In 1999, on the Feast of the Lord's Entrance into Jerusalem, a cross was installed on the dome of the Baptismal church. The construction of the second phase of the church complex continued, including a utility block.

In December 2001, the laying of piles for the third phase of construction, the main church of the Transfiguration of Christ with a bell tower, designed for 1,000 people, began. On the feast day of 2002, the cornerstone was consecrated at the foundation of the church. With the arrival of Bishop German to the throne in 2004, changes were made to the church project by architect Viktor Alexandrovich Vodyannikov, transforming it from a two-story building with two altars to a single-story building with three altars.

In August 2008, on the tenth anniversary of the first liturgy in the temporary church, a bell tower with seven bells was purchased with the funds of the parishioners, which was consecrated by Bishop German on the eve of the feast day.