Construction began in 1909,[2] the first service held in the cathedral in 1911, and it was added to the National Register of Historic Places in 1975.

Father John H. Kehler traveled from Virginia to the group of mining camps known as Denver City in January 1860 and delivered the first public services of the Episcopal Church in what would become Colorado Territory.

In 1908 a blind contest was held and the design of New York architectural firm of Tracy and Swartwout was selected.

The buttressed design was considered too expensive to build, so a redesign was requested which limited the cathedral to the nave and provided a temporary brick chancel.

United States Supreme Court Associate Justice Byron White was buried at St. John's Cathedral in 2002.