Known mainly as a character actor, Huddleston starred in the title role of 1985’s big-budget film Santa Claus: The Movie, which featured a top-billed Dudley Moore as an elf. One of Huddleston’s first roles came in the 1968 drama A Lovely Way to Die. Shortly afterward the actor became a frequent guest star on several of the leading television series of the 1960s and 1970s, among them, Adam-12, Then Came Bronson, Gunsmoke, Bewitched, Bonanza, Columbo, Cannon, McMillan & Wife, The Waltons, The Rookies, Medical Center, Kung Fu, Emergency!, Spencer’s Pilots, The Mary Tyler Moore Show, Police Woman, Hawaii Five-O, Walker, Texas Ranger, Charlie’s Angels, Sanford and Son, The Practice, and The Rockford Files. He appeared in many episodes of the TV series Petrocelli, as Lieutenant John Ponce during the series run from 1974 to 1976. He appeared in an unaired episode of the short-lived 1974 series The New Land and in the episode “The Nomads” from the 1977 series Quinn Martin’s Tales of the Unexpected (known in the United Kingdom as Twist in the Tale). He starred as J. T. Kallikak in the short-lived NBC situation comedy The Kallikaks later in 1977, and in 1979 he played the title role in the short-lived situation comedy Hizzonner as a small-town mayor. Among Huddleston’s notable feature film credits prior to Santa Claus: The Movie are his co-starring roles in Blazing Saddles, McQ, The Klansman, Smokey and the Bandit II and Breakheart Pass.

Huddleston resumed his television career with roles in various television movies, among them Heat Wave! (1974); The Oregon Trail (1976); Shark Kill (1976); Kate Bliss and the Ticker Tape Kid (1978); Family Reunion (1981); Computercide (1982); and M.A.D.D.: Mothers Against Drunk Drivers (1983). For much of the 1980s, Huddleston also starred in a series of television commercials for the Citrus Hill brand of orange juice. Huddleston’s post-Santa Claus career found him making occasional co-starring roles, in Spot Marks the X, Finnegan Begin Again, Frantic, Life with Mikey, The Big Lebowski in which he played the title role, and G-Men from Hell. Later, he also had a recurring role as Albert “Gramps” Arnold, the paternal grandfather of the protagonist in The Wonder Years. Huddleston appeared on Star Trek: The Next Generation as the train conductor in the episode “Emergence”. He also appeared twice on The West Wing as Max Lobell, a Republican Senator who allies with Jed Bartlet on the issue of campaign finance reform. His performance as Benjamin Franklin in a Boston stage production of 1776 is referenced in the book Assassination Vacation by Sarah Vowell, referring to him as “the actor who played The Big Lebowski in The Big Lebowski.” In 2009 he appeared in the thriller Locker 13. Huddleston was also featured in the 2010 special It’s Always Sunny in Philadelphia: It’s a Very Sunny Christmas released directly to DVD, Blu-ray and Digital Download.

On August 2, 2016, Huddleston died of heart and kidney disease in Santa Fe, New Mexico at the age of 85.