In the mid-1980s Cumming made brief appearances in Scottish television shows including Take The High Road and Taggart. His first major television role was in the Christmas 1991 comedy Bernard and the Genie, a Richard Curtis-scripted one-off show where he starred alongside Lenny Henry and Rowan Atkinson. Cumming starred as Sebastian Flight in the Scottish sitcom The High Life in 1994-5. The series was written by Cumming and co-star Forbes Masson, continuing an acting-writing partnership the two had developed since their drama school days. Masson and Cumming also formed a cult Kelvinside musical double act "Victor and Barry", which was filmed for an stv show and were nominated for a Perrier Award in the Edinburgh Festival Fringe in 1988, toured Australia in 1989, playing the Sydney Opera House, released a record ("See Victor and Barry and Faint") but were killed off onstage at the London Palladium in the early 1990s.
In 2001, he guest starred in the HBO comedy Sex and the City as O the designer in the episode, 'The Real Me'. Also in 2001 Cumming starred in [Spy Kids]. 2003 saw him playing a cameo role in the American sitcom Frasier, playing Niles' yoga instructor. He also guest starred on 3rd Rock from the Sun. In 2004, he starred in Showtime's Reefer Madness: The Movie Musical in which he played the role of The Lecturer – a versatile character who narrates the story and transforms himself into several other minor characters. Shortly afterward, he had a short role in Richard Bell's feature film Eighteen. In 2005 Alan played as Loki in Son of the Mask. He appeared in BBC show, Shoebox Zoo as the humble, kind-hearted Bruno.
Cumming played the role of Bill Blaikie, a gay drag queen party promoter hired by Kit Porter to manage her café cum nightclub, in season 3 of The L Word. His character had an affair with Max, a transgendered female-to-male character in the show. He appeared in episodes 2 to 7, which originally aired on Showtime in 2006. In 2007, Cumming played Glitch/Ambrose, an inventor whose brain had been partially removed, in the TV miniseries, Tin Man. He also provided the voice of Chuck Masters, a 50 year-old, paralyzed, HIV-positive gay man in Logo's Rick and Steve, a stop animation sitcom created by Q. Allan Brocka. He is also the host of the 2008–2010 seasons of the PBS Masterpiece Mystery! series.
Cumming also appeared as the third celebrity hijacker in Big Brother: Celebrity Hijack, giving the housemates a method acting task in which they had to stay in character all day and then produce an improvised play. He plays Eli Gold on the CBS television show The Good Wife, becoming a series regular in the show's 2010–2011 season, and Desrae, a transvestite, on the British series The Runaway. Cumming also hosted short-lived US cable television shows, "Eavesdropping with Alan Cumming," in which he interviewed female co-stars of his movie roles, and "Midnight Snack," where he and his dogs introduced cult movies. Cumming has also appeared on numerous US, UK and Australian talk shows.