Lasseter heard of a new character animation program at the California Institute of the Arts (often abbreviated as ‘CalArts’) and decided to follow his dream of becoming an animator. His mother further encouraged him to take up a career in animation, and in 1975 he enrolled as the second student (Jerry Rees was the first) in the CalArts Character Animation program created by Disney animators Jack Hannah and T. Hee. Lasseter was taught by three members of Disney’s Nine Old Men team of veteran animators—Eric Larson, Frank Thomas and Ollie Johnston—and his classmates included future animators and directors like Brad Bird, John Musker, Henry Selick, Tim Burton, and Chris Buck. During his time there, he produced two animated shorts—Lady and the Lamp (1979) and Nitemare (1980)—which each won the student Academy Award for Animation.

Upon graduating in 1979, Lasseter immediately obtained a job as an animator at Walt Disney Productions mostly due to his success with Lady and the Lamp. To put this into perspective, the studio had reviewed approximately 10,000 portfolios in the late 1970s in search of talent, then selected only about 150 candidates as apprentices, of which only about 45 were kept on permanently. In the fall of 1979, Disney animator Mel Shaw told the Los Angeles Times that “John’s got an instinctive feel for character and movement and shows every indication of blossoming here at our studios … In time, he’ll make a fine contribution.” At that same time, Lasseter worked on a sequence titled “The Emperor and the Nightingale” (based on The Nightingale by Hans Christian Andersen) for a Disney project called Musicana. Musicana was never released but eventually led to the development of Fantasia 2000.

Lasseter is a close friend and admirer of Japanese animator Hayao Miyazaki, whom he first met when TMS Entertainment sent a delegation of animators to the Disney studio in 1981 and showed a clip from Miyazaki’s first feature film, The Castle of Cagliostro (1979). Lasseter was so deeply moved that in 1985 he insisted on showing that clip and other examples of Miyazaki’s work after dinner to a woman he had just met (who would become his wife). He visited Miyazaki during his first trip to Japan in 1987 and saw drawings for My Neighbor Totoro (1988). After Lasseter became a successful director and producer at Pixar, he went on to serve as executive producer on several of Miyazaki’s films for their release in the United States and oversaw the translation and dubbing of their English language soundtracks. The gentle forest spirit Totoro from My Neighbor Totoro makes an appearance as a plush toy in Toy Story 3 (2010).

While putting together a crew for the planned feature, Lasseter had made some contacts in the computer industry, among them Alvy Ray Smith and Ed Catmull at Lucasfilm Computer Graphics Group. After being fired, and feeling glum knowing his employment with Disney was to end shortly, Lasseter visited a computer graphics conference in November 1983 at the Queen Mary in Long Beach, where he met and talked to Catmull again. Catmull inquired about The Brave Little Toaster, which Lasseter explained had been shelved. From his experience at Lucasfilm, Catmull assumed Lasseter was simply between projects since Hollywood studios have traditionally laid off employees when they lack enough productions to keep them busy. Still devastated at being forced out of the only company he had ever wanted to work for, Lasseter could not find the strength to tell Catmull that he had been fired.

Lasseter and his colleagues unknowingly stepped on some of their direct superiors’ toes by circumventing them in their enthusiasm to get the Where the Wild Things Are project into motion. The project was canceled while being pitched to two of Lasseter’s supervisors, animation administrator Ed Hansen, and head of Disney studios, Ron W. Miller, due to lack of perceived cost benefits for the mix of traditional and computer animation. A few minutes after the meeting, Lasseter was summoned by Hansen to his office. As Lasseter recalled, Hansen told him, “Well, John, your project is now complete, so your employment with the Disney Studios is now terminated.” Wilhite, who was part of Disney’s live-action group and therefore had no obligations to the animation studio, was able to arrange to keep Lasseter around temporarily until the Wild Things test project was complete in January 1984, but with the understanding there would be no further work for Lasseter at Disney Animation. The Brave Little Toaster would later become a 2D animated feature film directed by one of Lasseter’s friends, Jerry Rees, and co-produced by Wilhite (who had, by then, left to start Hyperion Pictures), and some of the staff of Pixar would be involved in the film alongside Lasseter.

After the short CGI film was presented at SIGGRAPH in the summer of 1984, Lasseter returned to Los Angeles with the hope of directing The Brave Little Toaster at Hyperion Pictures. He soon learned that funding had fallen through and called Catmull with the bad news. Catmull called back with a job offer, and Lasseter joined Lucasfilm as a full-time employee in October 1984 and moved to the Bay Area. after that, he worked with ILM on the special effects on Young Sherlock Holmes , where he made the first fully computer-generated photorealistic animated character, a knight composed of elements from a stained glass window. This effect was the first CG character to be scanned and painted directly onto film using a laser. Lasseter and Catmull’s collaboration, which has since lasted over thirty years, would ultimately result in Toy Story (1995), which was the first-ever computer-animated feature film.

Lasseter lives in Glen Ellen, California with his wife Nancy, a graduate of Carnegie Mellon University, whom he met at a computer graphics conference in San Francisco in 1985. Nancy majored in computer graphics applications, and for a short period of time was a stay at home mother and worked as a computer graphics engineer at Apple Computer. They married in 1988, and have four sons together in addition to Nancy’s son from a previous relationship, born between 1979/1980 and 1997.

Due to George Lucas’s financially crippling divorce, he was forced to sell off Lucasfilm Computer Graphics, by this time renamed the Pixar Graphics Group, founded by Smith and Catmull, with Lasseter as one of the founding employees. It was spun off as a separate corporation with Steve Jobs as its majority shareholder in 1986. Over the next 10 years, Pixar evolved from a computer company that did animation work on the side into an animation studio. Lasseter oversaw all of Pixar’s films and associated projects as executive producer. As well as Toy Story, he also personally directed A Bug’s Life (1998), Toy Story 2 (1999), Cars (2006), and Cars 2 (2011).

Disney announced that it would be purchasing Pixar in January 2006, and Lasseter was named the chief creative officer of both Pixar and Walt Disney Feature Animation, the latter of which he renamed Walt Disney Animation Studios. Lasseter was also named principal creative adviser at Walt Disney Imagineering, where he helped design attractions for Disney Parks. He oversaw all of Walt Disney Animation Studios’ films and associated projects as executive producer. He reported directly to Disney Chairman and CEO Bob Iger, bypassing Disney’s studio and theme park executives. He also received green-light power on films with Roy E. Disney’s consent.

In December 2006, Lasseter announced that Disney Animation would start producing animated shorts – 2D, CGI, or a combination of both – that would be released theatrically. Lasseter said he sees this medium as an excellent way to train and discover new talent in the company as well as a testing ground for new techniques and ideas.

In June 2007, Catmull and Lasseter were given control of Disneytoon Studios, a division of Walt Disney Animation Studios housed in a separate facility in Glendale. As president and chief creative officer, respectively, they have supervised three separate studios for Disney, each with its own production pipeline: Pixar, Disney Animation, and Disneytoon. While Disney Animation and Disneytoon are located in the Los Angeles area, Pixar is located over 350 miles (563 kilometers) northwest in the Bay Area, where Catmull and Lasseter both live. Accordingly, they appointed a general manager for each studio to manage day-to-day business affairs, then established a routine of spending at least two days per week (usually Tuesdays and Wednesdays) in Southern California.

He has won two Academy Awards, for Animated Short Film (Tin Toy), as well as a Special Achievement Award (Toy Story). Lasseter has been nominated on four other occasions—in the category of Animated Feature, for both Monsters, Inc. (2001) and Cars, in the Original Screenplay category for Toy Story and in the Animated Short category for Luxo, Jr. (1986)—while the short Knick Knack (1989) was selected by Terry Gilliam as one of the ten best animated films of all time. In 2008, he was honored with the Winsor McCay Award, the lifetime achievement award for animators.

On May 2, 2009, Lasseter received an honorary doctorate from Pepperdine University, where he delivered the commencement address.

Lasseter received a star on the Hollywood Walk of Fame in Hollywood in 2011, located at 6834 Hollywood Boulevard.

In November 2017, Lasseter took a six-month leave of absence after acknowledging allegations of workplace sexual misconduct that he described as “missteps” with employees in a memo to staff. The alleged misconduct towards employees included “grabbing, kissing, [and] making comments about physical attributes”. The alleged conduct became so well known that, according to Variety, at various times, Pixar had “minders who were tasked with reining in his impulses”.

In June 2018, Disney announced that Lasseter was leaving the company at the end of the year, taking a consulting role until then.

On January 9, 2019, Lasseter was hired to head Skydance Animation, which will produce animated films with Paramount Animation and Ilion Animation Studios. In a statement, Lasseter expressed his gratitude for the opportunity, adding “I have spent the last year away from the industry in deep reflection, learning how my actions unintentionally made colleagues uncomfortable, which I deeply regret and apologize for. It has been humbling, but I believe it will make me a better leader.”