Much like the history of the beloved Sunshine Cinema, which cycled from a church to a movie theatre with a couple of other uses in between, the IFC Center followed a similar path.

The original building at 325 Sixth Avenue was constructed as a Universalist church in 1831 and later housed St. Jude's Episcopal Free Church and the Union Reformed Church. In 1893 it became the home of J.&R. Lamb Studios. This firm was established in 1853 and stained glass, and later mosaics, marble, carved wood and metal pieces for churches, libraries, and private homes.

In 1937 the former church was converted into the Art Deco Waverly Theatre by architect Harrison Wiseman. The Waverly was immortalized in a song in the musical Hair and hosted the original long-running midnight showings of the Rocky Horror Picture Show.

Closed in 2001, the theatre reopened in 2005 as the IFC Center after another renovation, which added a new metal facade but retained the 150+-year-old gabled roof.