Pullman moved to New York in the early 1980s, and worked in regional and stock theater before landing a role in a 1985 revival of Sam Shepard's "Curse of the Starving Class". Pullman made his film debut as the world's dumbest crook in "Ruthless People" (1986) and followed with his first leading role, the hero of Mel Brooks' "Spaceballs" (1987). His dramatic lead was in Wes Craven's uneven "The Serpent and the Rainbow" (1988) and that same year he acted opposite William Hurt and Amy Wright in Lawrence Kasdan's "The Accidental Tourist". As Julian Hedge, the lovelorn book editor, Pullman set the pattern for many of his future roles, as the person who provides dependable emotional support. Several Pullman roles went unseen by the public at large: his turn as Burt Lancaster's son-in-law in "Rocket Gibraltar" (1988), as a brain surgeon in "Brain Dead" (1990) and as a sympathetic reporter in the flop musical "Newsies" (1992).

Things looked up somewhat with his role as Geena Davis' husband in Penny Marshall's "A League of Their Own" (1992) and as the plastic surgeon who talks Bridget Fonda out of breast implants in "Singles" (also 1992). In Nora Ephron's "Sleepless in Seattle" (1993), Pullman was cast in the traditional Ralph Bellamy role of the nice guy who loses the woman. "Malice" (1993) cast him as a college dean who runs afoul of a sinister surgeon (Alec Baldwin); although the role quaintly recalled his days as a college professor, he was still in second lead territory.

Stardom finally dawned with Pullman's romantic role opposite Sandra Bullock in "While You Were Sleeping" (1995). Not only did he get the girl, but Pullman turned in a sexy, casual and quietly witty performance. He next played Christina Ricci's "ghost therapist" dad in the children's fantasy "Casper" (also 1995). Pullman's comic talents were showcased as "Mr. Wrong" (1996), the obnoxious psycho who briefly charms Ellen DeGeneres in the unromantic comedy of that title. Two very atypical roles followed: as the President of the US in the sci-fi thriller "Independence Day" and as a convicted wife-killer in David Lynch's "Lost Highway" (both 1996). Subsequent roles include that of a neurotic but brilliant private investigator in Jake Kasdan's quirky "Zero Effect" (1998) and a supporting role as the lawyer who champions two young women imprisoned for drug trafficking in "Brokedown Palace" (1999). That same year he starred in the bomb "Lake Placid" and was featured in the similarly disappointing 2000 entry "Lucky Numbers."

The actor would continue to deliver solid performances in mainstream an indie films and TV movies, routinely serving up gems like his turn as Rory Culkin's schizophrenic father in the critical darling "Igby Goes Down" (2002), as a naval captain whose shipped is pressed into service following the Sept. 11 attacks in the Disney telepic "Tiger Cruise" (2004), and an opening sequence stint as one of the victims of a cursed Japanese home in the horror hit "The Grudge" (2004). He next appeared as a small town sheriff forced to contend with a group of teenagers who have formed a gang of pacifist gun enthusiasts suddenly turned violent in “Dear Wendy” (2005), scripted by Lars Von Trier. Pullman then showed up as the leader of a 19th century village in a parody of M. Night Shyamalan’s “The Village” (2004), one of many Hollywood movies getting the David Zucker treatment in “Scary Movie 4” (2006).

Pullman's TV career had begun in 1986 with a guest spot on "Cagney and Lacey" (CBS). He also appeared in the CBS movie "Home Fires Burning", with Holly Hunter in "Crazy in Love" (TNT, 1992), and on an episode of "Fallen Angels" (Showtime, 1995). Pullman has not neglected his stage work, either, appearing in productions with the Los Angeles Theater Center through 1989, and, in 1993, co-starring with Holly Hunter in "Control Freaks" at Hollywood's Met Theater.