In the early 19th century, the first wooden church dedicated to St. Nicholas the Wonderworker was built in Zabalka. It was located at the highest point in the area and initially served the military naval hospital. In 1819, the church was handed over to the diocesan authorities and became a parish church.

According to legend, in 1780, Prince G.A. Potemkin gifted an icon of St. Nicholas the Wonderworker to the old hospital church, which determined the name of the temple. In 1842, a stone church in the classical style was built in the center of the new market square, dedicated to St. Nicholas the Wonderworker. It was adorned with four-column porticos on the east and west, topped with a high dome on an octagonal drum and a two-tiered bell tower. The church was consecrated on May 9, 1842. During the Crimean War of 1853-1856, defenders of Sevastopol who died in Kherson hospitals were buried here.

Until 1917, an elementary school for children from the 'lower' social classes operated at the church. In the early years after the revolution, the church of St. Nicholas became the first renovationist church in Kherson, but this movement did not last long.

In the 1920s, the temple was plundered, and all church valuables were confiscated. At the end of 1929, the bells were removed, leaving only the small ones that remained in the narthex. In 1932, the church was closed and used as a grain warehouse, workshops, and a garage for tractors until 1941.

In 1941, the temple was reopened, and services resumed. Donations were collected, and local artists restored the iconostasis. That same year, artist Babenko created the icon of the Resurrection of Christ, the Shroud of the Mother of God, and the Crucifixion of the Lord. From 1949 to 1954, both chapels were restored. Nun Euphalia from the Kherson Annunciation Convent painted the icons for the side chapels, while nun Konstantia created the Theodorovsk and Kasperovsk icons of the Mother of God. Zinovia Osadcheva painted the icon of the Mother of God 'Quick to Hear,' which became the main shrine of St. Nicholas Naval Cathedral.

In May 2007, in honor of the 165th anniversary of its consecration, the St. Nicholas Church was granted the status of a Naval Cathedral. For this event, Archbishop John of Kherson and Tavria gifted the cathedral a relic of St. Nicholas the Wonderworker. In 2009, the bell tower was restored, and the dome was covered with golden bulat iron.

On May 22, 2015, Archbishop John consecrated a monument to St. Nicholas of Myra, installed in the cathedral's enclosure.