The church is first mentioned in sources from the second half of the 16th century as located in Murom, outside the city, opposite Nikola Mokry. According to tradition, the wooden temple in honor of St. Nicholas the Wonderworker was built at the behest of Ivan the Terrible, who visited Murom before his campaign against Kazan. In the 16th century, the church had two chapels: one for the martyr Theodore Stratilates and another for Saints Cosmas and Damian. Nearby was a wooden church in honor of the holy elders Zosimas and Savvatiy of Solovki. The Nikolskaya-Naberezhnaya church is also mentioned in the Inventory Book of Murom from 1636-1837 as a 'state building.' In 1700, the construction of the stone Nikolsky church began, initiated by Moscow priest Dmitry Khristoforov in memory of his father, archpriest Khristofor. In 1707, a decree was received for construction, and in 1714, an iconostasis was installed in the new church. In 1717, Murom icon painter Alexander Kazantsev created images of the twelve Sibyls, who foretold the birth of Jesus Christ, for the church. That same year, the church was consecrated. In 1803, a refectory with a chapel of the Descent of the Holy Spirit was added to the church, and in 1847, a new chapel in honor of the holy martyr Blasius, the patron of animals, appeared, as among the builders were the merchants Suzdaltsev-Ushakov, who traded livestock. The church was closed in 1940, and in the 1950s-1960s, it housed a poultry factory. In the late 1960s, the building was transferred to the city museum, which planned to create an exhibition about the Oka River and a display of wooden sculpture. In the following years, the church stood empty. In 1991, the church was handed over to the Vladimir-Suzdal Diocese for the resumption of services. On July 9, 1993, the relics of the holy righteous Juliana Lazarevskaya were transferred to the church, becoming its main shrine. Before the revolution, the church housed a revered 14th-century icon of St. Nicholas the Wonderworker, which now belongs to the Murom Museum.

The Nikolsky church is an example of local interpretation of 'Moscow Baroque,' which is evident in its decor, while the five-domed structure remains traditional. The only unusual feature is the dome completion of the bell tower with round windows. Throughout its existence, the church has not been rebuilt due to the poverty of the parish. The carved iconostasis was preserved in its original form until the 1960s. The Church of St. Nicholas the Wonderworker was traditionally built by the water, as St. Nicholas was venerated as the savior of drowning people and the patron of travelers. During the spring flood, when the waters of the Oka approach the hill on which the church stands, the people of Murom say: 'Nicholas has wet feet.'