The three-altar Holy Spirit Church in Kherson was laid in 1804. The front part of the temple was built in one summer thanks to a donation of 15 thousand rubles. However, construction then stopped due to lack of funds and was completed only in 1835. In January 1836, the northern chapel was consecrated in honor of the Holy Martyrs of Chersonesus and the southern chapel in honor of Archangel Michael. The main altar was consecrated on August 16, 1836, by Archbishop Gabriel Rozanov. According to him, significant assistance in construction was provided by Kherson merchants Galukhin, Bogdanov, Sikachev, and Nosov, which is confirmed by local tradition calling the church "merchant's."

The church is located near the city market, which is why it received the name "imported," a name that has persisted to this day. Initially, the temple had the shape of a square cross with a colonnade and a low dome. 80 meters to the west of it, a five-tiered bell tower was built, consecrated on August 6, 1806, which served as a parish church under the name of the Transfiguration. It burned down on August 19, 1941, on the day of the Transfiguration of the Lord, and was dismantled in the post-war years. Now, a chapel with an eternal lamp stands in its place.

In 1907, a refectory was added to the church, extending the building. Sunday discussions and choir rehearsals were held in the basement of the refectory. The builders of the refectory are said to be the merchants Irlikovs. The Holy Spirit Church was considered the richest and most beautiful in the city, with gilded iconostases and church utensils.

In 1922, church valuables were seized from the temple, and from 1926 to 1937 it was under the Renovationists. After that, the temple was used as a flour warehouse until 1944. At the end of 1941, a church in honor of the Transfiguration of the Lord was arranged in the basement of the refectory. In 1944, the temple was returned to the believers, who began its restoration. The chapels were restored and consecrated, but the ancient paintings did not survive.

Until 1945, the cathedral of Kherson was the Assumption Cathedral, then the Catherine Cathedral. In 1947, the Holy Spirit Church became the cathedral. From 1953 to 1960, the rector was Archpriest Boris Georgievich Stark, who decorated the cathedral and installed new iconostases. In 1955-1956, Odessa artists painted new icons for the cathedral.

Until 1995, there was no bell tower in the cathedral; eight small bells were used. The area of the cathedral is 1441 sq.m, the height of the walls is 9.7 m, and the height of the dome is 19.7 m.

In 1991, the Kherson Diocese was formed, with Metropolitan Leonty Gudimov as the first hierarch. Under Bishop Hilarion Shukalo, the lower Transfiguration chapel was expanded and consecrated, and a new bell tower was built. Restoration continued under subsequent hierarchs.

The main relics of the cathedral include the miraculous copy of the Kasperskaya Icon of the Mother of God, the Not-Made-By-Hands Image of the Savior, the Theodorovskaya and Pochaev Icons of the Mother of God, icons of Saint Nicholas and other saints. The graves of Archpriests Leonid Bogdanov and Ioann Karlev are located in the cathedral's enclosure.