Upon graduating from the University of Minnesota, Peter MacNicol traveled the length and breadth of the U.S. as a regional repertory actor. In his first film, Dragonslayer (1981), MacNicol essayed one of his few leading-man roles as Galen, a hapless assistant sorcerer who makes good. His most celebrated film assignment was as Stingo, the innocent-bystander narrator of Sophie's Choice. Most of the time, MacNicol has been seen in comical, sycophantic roles, such as the easily demonized Janocz in Ghostbusters II (1989) and the unctuous camp counselor in Addams Family Values (1993). On television, Peter MacNicol starred in the brief Norman Lear political lampoon The Powers That Be (1992) and co-starred as Alan Birch on the CBS medical drama Chicago Hope (1994).
MacNicol continued to play small but indelible roles in a variety of small but indelible films throughout the mid-'90s. There was 1992's underrated Housesitter with Goldie Hawn and Steve Martin; acclaimed director Mel Brooks' Dracula: Dead and Loving It (1995); and a starring role opposite cult comedian Rowan Atkinson in 1997's Bean. Despite his respectable feature-film success, however, MacNicol wouldn't get solid mainstream recognition until the 1997 debut of Ally McBeal. The show featured MacNicol as John Cage, an immensely insecure but highly gifted lawyer whose lovable, if over-sensitive, nature tugged at the heartstrings of Ally (Calista Flockhart) and television audiences alike. MacNicol remained a lead character on the show from 1997 to 2002, and was able to participate not just as an actor, but also as a director, screenwriter, and amateur karaoke singer. No longer the affable John Cage, MacNicol could be seen assigning Jamie Foxx the unpleasant task of letting his employees know of a rapidly approaching downsizing in 2004's Breakin' All the Rules. Recurring roles on Numbers and 24 as well as voice work in such animated shows as Harvey Birdman, Attorney at Law, The Batman, The Spectacular Spider-Man helped MacNicol maintain a high profile in the following years, and in 2012 he could be seen as the Secretary of Defense in the big-budget game board adaptaion Battleship.