In 1952, several families in Denver decided to create a Russian Orthodox church. Among them were a stonemason, a carpenter, a former lighthouse keeper, a technical translator, a retired farmer, an editor, an engineer, a retired military officer, and others. These people, despite the difficulties, actively took on the task.

Initially, services were held in a private home. In the fall of 1952, a small house on King Street in west-central Denver was purchased for $3,000. Over time, the community grew, and in 1966, one of the parishioners found a suitable building for relocation. A plot in a good area of the city, near the University of Denver, was bought, and thanks to the joint efforts of the parishioners, the building was moved to the new location. The church still stands there, symbolizing the unwavering faith of the first parishioners.

The icons on the iconostasis were painted by the late parishioner Lev Lominago. The fresco on the back wall was done by Archimandrite Alipiy of Chicago, while the side walls were painted by Archimandrite Alipiy and Hieromonk Grigory.

Metropolitan Anastasy, the primate of the Russian Orthodox Church Outside Russia at that time, often visited the parish in its early years. The first priest was Archpriest Panteleimon Khaplanov, who served from 1952 to 1955. Over the years, the rectors included Archpriest Ioann Obletilov (1955-1956), Archpriest Boris Kritsky (1956-1967), Archpriest Peter Burlakov (1967-1985), Priest Alexey Yang (1985-1987, 1993-2000), Priest Justin Grouse (1988-1992), Priest Stefan Allen (1992-2000), and Archpriest Boris Henderson (since 2000). From 1969 to 1996, Protopriest Ioann Ivanov faithfully served in the parish. Priest Ioann Veselak served here from 1998 to 2019. Since 2007, Priest Mikhail Preobrazhensky has been serving in the parish.