The wooden Nikolskaya Church was built in Yakutsk in 1718 and became one of the first in the city. It was located behind the Town Hall square, near the fortress. In the mid-18th century, the Church of St. Nicholas the Wonderworker was mentioned along with almshouses.

Over time, the wooden building likely deteriorated or burned down, and in 1791, residents began constructing a new stone church. Due to a lack of funds, the construction lasted more than thirty years. The church was built on the site where the Institute of Geology of the Yakut Scientific Center later stood. By the autumn of 1821, the upper floor was completed, and three upper altars were consecrated. However, after an earthquake, the foundation proved unstable, leading to the destruction of walls and the appearance of cracks. A commission found that the builder had not paid proper attention to the foundation. In 1834, the Yakut regional government received an order from Irkutsk to dismantle the church walls. It is known that the lower floor had 18 windows, the upper floor had 20 windows, and the tall square consisted of two floors with six altars. The church had 9 bells, including a large and polyelai bell weighing 66 poods and 18 pounds.

The idea of building a new Nikolsky cemetery church for burial rites was proposed by merchant Ivan Yakovlevich Shilov and supported by the townspeople, who raised funds through donations. In the summer of 1843, Archbishop Nil Isakovich of Irkutsk visited Yakutsk and supported the initiative. The city began producing bricks and extracting stone, and stonemason crews formed. On May 9, 1847, the foundation was consecrated, and by 1851, the construction of the church was mostly completed. Merchant Shilov oversaw the construction, chose the site, and purchased materials. In 1852, Archbishop Innocent Veniaminov of Kamchatka consecrated the main altar, and later two more were consecrated. The new church received bells, vestments, and icons from the old one. All three iconostases were created according to the drawings of architect Diakonov. People from different social classes were buried in the churchyard. Merchant Ivan Yakovlevich Shilov Jr. was buried at the entrance to the church for his benefactions.

In the 1920s, the Nikolskaya Church became known due to the shootings of representatives of the intelligentsia, merchant class, and clergy in its yard. The church was handed over to the Renovationists, and in the 1930s, its bells were removed. By the end of the decade, city construction approached the cemetery, which began to be demolished. Monuments were stolen, and by 1939, the church remained the last functioning one in Yakutsk but was closed due to "emergency condition."

After its closure, the church was partially rebuilt and underwent major repairs. It housed the party archive, the city architecture office, and a library collector, which helped preserve the building. In 1945-1946, believers were allocated a prayer house instead of the church. In the 1950s, the cemetery was leveled, and gravestones were used in construction, for example, as the foundation for the city power station. In 1976, the church was included in the list of architectural monuments, and in 1982, cosmetic repairs were carried out. By the end of the Soviet period, the church retained its original appearance and volumes.

In the early 1990s, the church was returned to the believers. Patriarch Alexy II visited the church in 1993 and expressed hope for its restoration. The government of Yakutia allocated funds for restoration, and on October 8, 1995, the church was consecrated again, becoming the cathedral of the Yakut diocese. It retained this status until 2005 when it became a parish church named "Gradoyakutsky." In the 2010s, under the guidance of D. A. Trofimov, the interior decoration of the church was updated.