In 1887, an independent Orthodox parish was established on the Commander Islands. At that time, there was no full-fledged church on the islands, only a few old chapels. To build a new church, which was planned to start in the spring of 1888, timber was brought from America. Construction continued until 1892. This year marked the anniversary of the miraculous rescue of Tsarevich Nicholas, and the village had been called Nikolsk since the 1880s. The old chapel was consecrated in 1842 by Bishop Innocent (Veniaminov) in honor of St. Innocent of Irkutsk, who was considered the patron saint of the village. Therefore, the new church was consecrated in honor of St. Nicholas the Wonderworker and St. Innocent of Irkutsk. A few years later, another church was built in the village of Preobrazhenskoe on Medny Island, modeled after the Nikolsk-Innocentiev church. In the 1920s, both churches were closed. The Spaso-Preobrazhensky church was dismantled in the 1930s. The Nikolsk-Innocentiev church was repurposed as a village club, then as a dormitory and an art school. In 1983, the building of the former church burned down.

In 1991, the remains of Vitus Bering and five participants of the Second Kamchatka Expedition were found on the Commander Islands. They were sent to Moscow, where after research it was decided to reinter them on Bering Island. Father Yaroslav Levko arrived for this purpose and held a memorial service for the deceased sailors. This was the first church service on the island since 1926. In 2009, a local Orthodox community was registered with the Ministry of Justice, and discussions began about building a church.

On September 17, 2010, Patriarch Kirill visited the Commander Islands and consecrated the site for the new church. A year later, the foundation of the church was consecrated, and on November 3, 2011, a dismantled church was delivered to the island. It was transported by rail from Kirov to Vladivostok. Craftsmen from Vyatka assembled the church on-site over eight weeks. In September 2012, an iconostasis created by artists from the Abramtsevo workshop in Sergiev Posad was installed in the church. The Aleutian Regional Museum returned the bell of the Nikolsk-Innocentiev church, which was cast in 1891 in St. Petersburg at the V. Orlov factory. On October 27, 2012, Bishop Artemy of Petropavlovsk and Kamchatka consecrated the church.