After beginning his acting career with a play, Stiller wrote several mockumentaries, and was offered two of his own shows, both entitled The Ben Stiller Show. He began acting in films, and had his directorial debut with Reality Bites. Throughout his career he has since written, starred in, directed, and/or produced over fifty films including Heavyweights, There's Something About Mary, Meet the Parents, Zoolander, Dodgeball, and Tropic Thunder. In addition he has had multiple cameos in music videos, television shows, and films.

Stiller is a member of the comedic acting brotherhood colloquially known as the Frat Pack. His films have grossed more than $2.1 billion worldwide, with an average of $73 million per film. Throughout his career, he has received several awards and honors including an Emmy Award, several MTV Movie Awards, and a Teen Choice Award.

Stiller was born in New York City. His father, Jerry Stiller, is Jewish, and his mother Anne Meara, who is of Irish Catholic background, converted to Judaism after marrying his father. His parents frequently took him on the sets of their appearances, including an appearance on The Mike Douglas Show when he was six. He admitted in an interview that he considered his childhood unusual: "In some ways, it was a show-business upbringing—a lot of traveling, a lot of late nights—not what you'd call traditional." His sister, actress Amy Stiller, has made appearances in many of his productions, including Reality Bites, Dodgeball: A True Underdog Story, and Zoolander.

He displayed an early interest in film making and made Super 8 movies with his sister and friends. At 10 years old, he made his acting debut as a guest on his mother's television series Kate McShane. In the late 1970s he performed with the New York City troupe NYC's First All Children's Theater, performing in several roles, including the title role in Clever Jack and the Magic Beanstalk. After being inspired by the television show Second City Television while in high school, Stiller realized that he wanted to get involved with sketch comedy.

Stiller attended the Cathedral School in and graduated from the Calhoun School in New York in 1983. He started performing on the cabaret circuit as opening act to the cabaret siren Jadin Wong. Stiller then enrolled as a film student at the University of California, Los Angeles. After nine months, Stiller left school to move back to New York City. He made his way through acting classes, auditioning, and trying to find an agent.

Stiller landed a role in the Broadway revival of John Guare's The House of Blue Leaves, alongside John Mahoney; the production would garner four Tony Awards. During its run, Stiller produced a satirical mockumentary whose principal was fellow actor Mahoney. His comedic work was so well received by the cast and crew of the play that he followed up with a 10 minute short called The Hustler of Money, a parody of the Martin Scorsese film The Color of Money. The film featured him in a send-up of Tom Cruise's character and Mahoney in the Paul Newman role, only this time as a bowling hustler instead of a pool shark. The short got the attention of Saturday Night Live, which aired it in 1987, and two years later offered him a spot as a writer. In the meantime, he also had a bit part in Steven Spielberg's Empire of the Sun.

In 1989, Stiller wrote and appeared on a season of Saturday Night Live as a featured performer. However, since the show did not want him to make more short films for the show, he left after five shows. He then put together Elvis Stories, a short film about a fictitious tabloid focused on recent sightings of Elvis Presley. The film starred friends and co-stars John Cusack, Jeremy Piven, Mike Myers, Andy Dick, and Jeff Kahn. The film was considered a success, and led him to develop another film entitled Back to Brooklyn for MTV.

MTV was so impressed with Back to Brooklyn that they offered Stiller a 13-episode show in the experimental "vid-com" format. Entitled The Ben Stiller Show, this series mixed comedy sketches with music videos and parodied various television shows, music stars, and films. It starred Stiller, along with main writer Jeff Khan and Harry O'Reilly with occasional appearances by his parents Jerry Stiller and Anne Meara, and sister Amy Stiller.

Although the show was canceled after its first season, it led to another show entitled The Ben Stiller Show on the Fox Network in 1992. The Ben Stiller Show aired 12 episodes on Fox, with a 13th unaired episode broadcast by Comedy Central in a later revival. Among the principal writers on The Ben Stiller Show were Stiller and Judd Apatow, with the show featuring the ensemble cast of Stiller, Janeane Garofalo, Andy Dick, and Bob Odenkirk. Both Denise Richards and Jeanne Tripplehorn appeared as extras in various episodes. Throughout its short run, The Ben Stiller Show frequently appeared at the bottom of the ratings, even as it garnered critical acclaim and eventually won the Emmy for "Outstanding Individual Achievement in Writing in a Variety or Music Program" after it was canceled.

After a few minor film roles in the early 1990s, such as Stella, Highway to Hell, and a cameo in The Nutt House, Stiller devoted his time to writing, fund raising, recruiting cast members, starring in, and directing Reality Bites. The film was produced by Danny DeVito (who later directed Stiller's 2003 film Duplex and produced the 2004 film Along Came Polly). Reality Bites debuted as the highest-grossing film in its opening weekend and received mixed reviews.