The church is located on the site of the ancient Trinity Men's Monastery, which was known since 1626. The main temple of the monastery was dedicated to the Life-Giving Trinity and had an altar in honor of St. Alexander of Svir. It was popularly called the "Black Trinity" to distinguish it from the nearby parish church known as the "White Trinity."

After Catherine the Great's decree on the establishment of monastic states, the monastery was closed, and its churches became parish churches. By that time, the Trinity temple had significantly deteriorated, making it almost impossible to serve in it. Priest Panteleimon Ivanov, along with parishioners, appealed to the church authorities for permission to build a new stone church. Permission was granted on March 28, 1766. The construction of the new temple took about 15 years, and the main altar was consecrated in 1777. In 1833, the church was renamed the Holy Spirit Church to distinguish it from the neighboring Trinity Church, the "White Trinity." The parish was always poor and was even attached to others several times. The main street Golodaevka, now Proletarskaya, explains the reason for this.

After the revolution, on May 8, 1929, the church was one of the first in the city to be closed and repurposed as a printing house for the Promkombinat. The bell tower was partially destroyed, the dome was demolished, and the building itself was altered with extensions. In 1995, the printing house was moved to a new building, and the church was handed over to the community of believers "Cypress." The disfigured temple needed major repairs. The first service took place on December 17, 1995, on the feast of St. Barbara the Great Martyr. The rector of the church, a young priest and graduate of the Moscow Theological Seminary, Sergey Zhulin, needed a lot of effort to restore the beauty of the House of God.

Despite the difficult conditions for conducting services, the Holy Spirit Church became one of the favorites in the city. A Sunday school for children was opened within the community of believers, and catechetical courses were held.