He studied literature in college with aspirations of becoming a writer. He left midway through his stint in college to work on an off-shore oil rig in the Gulf of Mexico. While working on the rig he read a lot of literature, but on land he developed a love of film through repeated visits to a repertory theater in Houston. It was at this point that Linklater realized he wanted to be a filmmaker. After his job on the oil rig, Linklater used the money he had saved to buy a Super-8 camera, a projector, some editing equipment, and moved to Austin. It was here that the aspiring cineaste founded a film society at the University of Texas at Austin and grew to appreciate such stylized auteurs like Robert Bresson, Yasujiro Ozu, Nagisa Oshima, and Josef Von Sternberg.

For several years Linklater made many short films that were, more than anything, exercises and experiments in film techniques. Finally, he completed his first feature, the rarely seen It's Impossible to Learn to Plow by Reading Books, a Super-8 feature that took a year to shoot and another year to edit. The film is significant in the sense that it establishes most of Linklater's preoccupations. Stylistically, the film contains his trademark minimal camera movements and lack of narrative, while thematically it examines the notions of traveling with no real particular direction in mind. These idiosyncrasies would be explored in greater detail in future projects.

To this end, Linklater created Detour Films (a homage to the 1945 low budget film noir by Edgar G. Ulmer), and subsequently made Slacker for only $23,000. The film is an aimless day in the life of the city of Austin, Texas by showcasing its more eccentric characters.

He is best known for his independent films, which feature characters having philosophical discussions. He also founded the Austin Film Society in 1985, and is lauded for launching and solidifying the city of Austin as a hub for independent filmmaking.

Many of Linklater's films take place in one day, a technique that has gained popularity in recent years. Slacker, Dazed and Confused, Before Sunrise, and Before Sunset are examples of this method.

In 2005, he was nominated for an Academy Award for Best Adapted Screenplay for his film Before Sunset.

Two of his most recent films (A Scanner Darkly and Waking Life) both display a similar animated style. To create this effect, Linklater shot and edited both movies into a completed live-action state, then employed a team of artists to 'trace over' individual frames (a technique known as rotoscoping). The result is a distinctive 'semi-real' quality, praised by such critics as Roger Ebert (in the case of Waking Life) as being original and well-suited to the aims of the film.

Despite his popularity and ability to direct high paying Hollywood productions, Linklater remains in Texas, with his own studio there to run most of his film productions. This is similar to Robert Rodriguez, who is also a Texan film maker that refuses to live or work in Hollywood for any extended period of time. In 2004 the British television network Channel 4 produced a major documentary about Linklater in which the film maker frankly discussed the personal and philosophical ideas behind his films. "St Richard of Austin" was presented by Ben Lewis and directed by Irshad Ashraf and broadcast on Channel 4in December 2004 in the UK.