Earlier work in film included model-making, prosthetic make-up and concept illustrations for Hardware and Dust Devil for Director Richard Stanley; work on Nightbreed for Clive Barker; and on Alien for David Fincher. Between 1990 and 1992, he contributed the occasional cover painting and strip to Judge Dredd Megazine, working under the pseudonym "Chris Halls"; Halls is his stepfather's surname.

After seeing Cunningham's work on the 1995 film version of Judge Dredd, Stanley Kubrick head-hunted Cunningham to design and supervise animatronic tests of the central robot child character in his version of the film A.I. Artificial Intelligence. Cunningham worked for over a year on the film before leaving to pursue a career as a Director.

In an August 1999 Spike Magazine interview, Gibson stated "He (Chris) was brought to my attention by someone else. We were told, third-hand, that he was extremely wary of the Hollywood process, and wouldn't return calls. But someone else told us that Neuromancer had been his Wind In The Willows, that he'd read it when he was a kid. I went to London and we met." Gibson is also quoted in the article as saying "Chris is my own 100 per cent personal choice...My only choice. The only person I've met who I thought might have a hope in hell of doing it right. I went back to see him in London just after he'd finished the Bjork video, and I sat on a couch beside this dead sex little Bjork robot, except it was wearing Aphex Twin's head. We talked."

In 2000, Cunningham and cyberpunk author william Gibson began work on the script for Gibson's 1984 novel Neuromancer. However, because Neuromancer was due to be a big budget studio film, it is rumoured that Cunningham pulled out due to being a first time Director without final cut approval. He also felt that too much of the original book's ideas had been cannibalised by other recent films.

It is rumoured that the character of Damien Pease in Gibson's 2003 novel Pattern Recognition was based on Cunningham, with the character's apartment featuring a female robot which had appeared in one of Cunningham's videos.

The video collection The Work of Director Chris Cunningham was released in November 2004 as part of the Directors Label set. This DVD includes selected highlights from 1995–2000.

In 2005, Cunningham released the short film Rubber Johnny as a DVD accompanied by a book of photographs and drawings. Rubber Johnny, a six-minute experimental short film cut to a Soundtrack by Aphex Twin, remixed by Cunningham was shot between 2001 and 2004. Shot on DV night-vision, it was made in Cunningham's own time as a home movie of sorts, and took three and half years of weekends to complete. The Telegraph called it "like a Looney Tunes short for a generation raised on video nasties and rave music".

In December 2007 Cunningham produced two tracks, "Three Decades" and "Primary Colours", for Primary Colours, the second album by The Horrors. In the summer of 2008, due to scheduling conflicts with his feature film script writing he could not work on the rest of the album which was subsequently recorded by Geoff Barrow from Portishead.

In November 2008, Cunningham followed on with another photoshoot for Vice Magazine.

In 2005, Cunningham played a 45-minute audio visual piece performed live in Tokyo and Osaka in front of 30,000+ fans over the two nights at Japan’s premier electronic music event Electraglide. These performances evolved into Chris Cunningham Live, a 55 minute long performance piece combining original and remixed music and film. It features remixed, unreleased and brand new videos and music dynamically edited together into a new live piece spread over three screens. The sound accompanying these images includes Cunningham’s first publicly performed compositions interspersed with his remixes of other artist’s work. Chris Cunningham Live debuted as one of the headline attractions at Warp 20 in Paris on 8 May 2009 with other performances scheduled at festivals in UK, and a number of European cities later in the year. Chris Cunningham Live continued in June 2011, with performances in London, Barcelona, and Sydney, Australia.