The band was created by Kevin Barnes and named after a failed romance with a woman from Montreal, though the story changes in various interviews. Barnes was the only member of the "group" prior to his relocation to Athens, Georgia. There, he met Derek Almstead, later of the Circulatory System, M Coast, Elf Power etc., and Bryan Poole, who also performs as The Late B.P. Helium. Together, they recorded their first album, Cherry Peel, as well as The Bird Who Ate the Rabbit's Flower and The Bedside Drama: A Petite Tragedy.

After production on The Gay Parade began in 1998, Poole left the band to focus on his duties with Elf Power, another Elephant Six band from Athens. Barnes then recruited Jamey Huggins and Dottie Alexander, who had been performing together as Lightning Bug vs. Firefly, to play various instruments. Derek moved from drums to bass. The band was joined soon after by Marshmallow Coast's Andy Gonzales.

A number of singles and a re-release of The Bird Who Continues to Eat the Rabbit's Flower occurred before the advent of the band's third album, The Gay Parade in 1999. With contributions from several members of the Elephant Six collective at the time, it also featured artwork from Kevin's brother David Barnes, who would continue to do artwork for future albums.

Following the release of The Gay Parade, the band signed with Kindercore Records, who would release a number of singles and compilations. It wasn't until 2001 that Coquelicot Asleep in the Poppies: A Variety of Whimsical Verse would be released as a new album with original material. The album again featured contributions from across the Elephant Six spectrum.

Of Montreal front figure Kevin Barnes playing inGothenburg, Sweden in 2005

Of Montreal's next album, Skeletal Lamping, was released on October 21, 2008. It was released in ten different formats, including conventional CD and vinyl, as well as t-shirts, button sets, wall decals, tote bags, and a paper lantern, the latter formats replete with a digital download code for the album.  All items for the collection were designed by The Bee With Wheels (David Barnes) and Gemini Tactics (Nina Barnes). In an essay addressing the concept behind the album's release, Kevin Barnes stated, "We feel that there's no reason to produce another object that just sits on a shelf. We only want to produce objects that have a function and that can be treasured for their singularness."[6] In an interview with NPR, Kevin Barnes revealed that the concept of the CD may be going the way of the 8-track in favor of MP3 downloads. David Barnes joked that fans would buy the album via MP3 download and the version that comes with an amazing sandwich.[7] The album reached number one on emusic's Most Downloaded Albums Chart.[8] The video for the album's second single, "An Eluardian Instance", was directed by Jesse Ewles.

The Band will be @ Firestone Live 4/10/10