Built from 1895 to 1896, the church was the second Orthodox church at the site, replacing the 1849 structure. The church was built from logs in the Pskov style—in the shape of a ship. The bell tower was completed later in 1900.

The Chapel of St. Nicholas was built in 1906. It rests over the graves of Igumen Nikolai, his assistant and reader Makari Ivanov, and an unrecorded monk. The chapel sits on the site of the original chapel, across the street from the church, on a bluff overlooking the confluence of the Kenai River and Cook Inlet. The rectory was built in 1881 and is considered the oldest building in the Peninsula.

The church site, including the rectory, cemetery, and chapel, was declared a National Historic Landmark in 1970. It is the oldest standing Orthodox church in Alaska.