In 1989, Abrams met Steven Spielberg at a film festival, where Spielberg spoke about a possible Who Framed Roger Rabbit sequel, with Abrams as a possible writer and with Robert Zemeckis as producer. Nothing came up from this project, although Abrams has some storyboards for a Roger Rabbit short.

In 1994, he was part of the “Propellerheads” with Rob Letterman, Loren Soman, and Andy Waisler, a group of Sarah Lawrence alums experimenting with computer animation technology. They were contracted by Jeffrey Katzenberg to develop animation for the film Shrek. Abrams worked on the screenplay for the 1998 film Armageddon with producer Jerry Bruckheimer and director Michael Bay. That same year, he made his first foray into television with Felicity, which ran for four seasons on The WB Network, serving as the series’ co-creator (with Matt Reeves) and executive producer. He also composed its opening theme music.

Under his production company, Bad Robot, which he founded with Bryan Burk in 2001, Abrams created and executive-produced ABC’s Alias and is co-creator (along with Damon Lindelof and Jeffrey Lieber) and was executive producer of Lost. As with Felicity, Abrams also composed the opening theme music for Alias and Lost. Abrams directed and wrote the two-part pilot for Lost and remained active producer for the first half of the season. Also in 2001, Abrams co-wrote and produced the horror-thriller Joy Ride. In 2006, he served as executive producer of What About Brian and Six Degrees, also on ABC. He also co-wrote the teleplay for Lost’s third-season premiere “A Tale of Two Cities” and the same year, he made his feature directorial debut with Mission: Impossible III, starring Tom Cruise. Abrams spoke at the TED conference in 2007.

In July 2002, Abrams wrote a script for a possible fifth Superman film entitled Superman: Flyby. Brett Ratner and McG entered into talks to direct, although Abrams tried to get the chance to direct his own script. However, the project was finally cancelled in 2004 and instead Superman Returns was released in 2006.

In 2008, Abrams produced the monster movie Cloverfield, which Matt Reeves directed. In 2009, he directed the science fiction film Star Trek, which he produced with Lost co-creator Damon Lindelof. While it was speculated that they would be writing and producing an adaptation of Stephen King’s The Dark Tower series of novels, they publicly stated in November 2009 that they were no longer looking to take on that project. In 2008, Abrams co-created, executive produced, and co-wrote (along with Roberto Orci and Alex Kurtzman) the FOX science fiction series Fringe, for which he also composed the theme music. He was featured in the 2009 MTV Movie Awards 1980s-style digital short “Cool Guys Don’t Look at Explosions”, with Andy Samberg and Will Ferrell, in which he plays a keyboard solo. NBC picked up Abrams’s Undercovers as its first new drama series for the 2010–11 season. However, it was subsequently cancelled by the network in November 2010.

In 2008, it was reported that Abrams purchased the rights to a New York Times article “Mystery on Fifth Avenue” about the renovation of an 8.5 million dollar co-op, a division of property originally owned by E. F. Hutton & Co. and Marjorie Merriweather Post, for six figures and was developing a film titled Mystery on Fifth Avenue, with Paramount Pictures and Bad Robot Productions, and comedy writers Maya Forbes and Wally Wolodarsky to write the adaptation. According to the article, a wealthy couple Steven B. Klinsky and Maureen Sherry purchased the apartment in 2003 and live there with their four children. Soon after purchasing the apartment, they hired young architectural designer Eric Clough, who devised an elaborately clever “scavenger hunt” built into the apartment that involved dozens of historical figures, a fictional book and a soundtrack, woven throughout the apartment in puzzles, riddles, secret panels, compartments, and hidden codes, without the couple’s knowledge. The family didn’t discover the embedded mystery until months after moving into the apartment. After Abrams purchased the article, Clough left him an encrypted message in the wall tiles of a Christian Louboutin shoe store he designed in West Hollywood.

In November 2009, it was reported that Abrams and Bad Robot Productions were producing, along with Cartoon Network Movies, Warner Bros., Frederator Films and Paramount Pictures, a film adaptation of Samurai Jack. However, in June 2012, series creator Genndy Tartakovsky stated that the production of the film was scrapped after Abrams’ departure from the project to direct Star Trek. For this and other reasons, Tartakovsky decided to make a new season instead of a feature film. Also in 2009, it was reported that Abrams and Bad Robot Productions would produce a film based on the Micronauts toy line. However, a film has never gone into production.

Abrams wrote and directed the Paramount science fiction thriller Super 8, starring Joel Courtney and Elle Fanning, while co-producing with Steven Spielberg and Bryan Burk; it was released on June 10, 2011.

Abrams will produce and Guillermo del Toro will write and direct a science-fiction action/thriller film titled Zanbato, which Abrams has been working on since 2011.

Abrams directed the sequel to Star Trek, Star Trek Into Darkness, released in May 2013. The film was interpreted as a loose remake of Star Trek II: The Wrath of Khan. Critics generally reacted positively to the film, while Nicholas Meyer, the director of The Wrath of Khan, called it a “gimmick”. Abrams was criticized for the film’s treatment of classic villain Khan Noonien Singh (Benedict Cumberbatch). Many felt that much of the character, originally played by Mexican actor Ricardo Montalban, had been lost, especially his ethnic identity. Two years after the film’s release, Abrams said of the film, “there were certain things I was unsure of. … Any movie … has a fundamental conversation happening during it. And [for Into Darkness,] I didn’t have it… [The weakness of the plot] was not anyone’s fault but mine. … [The script] was a little bit of a collection of scenes that were written by my friends … And yet, I found myself frustrated by my choices, and unable to hang my hat on an undeniable thread of the main story. So then I found myself on that movie basically tap-dancing as well as I could to try and make the sequences as entertaining as possible. … I would never say that I don’t think that the movie ended up working. But I feel like it didn’t work as well as it could have, had I made some better decisions before we started shooting.”

On January 25, 2013, The Walt Disney Studios and Lucasfilm officially announced Abrams as director and producer of Star Wars: The Force Awakens, the seventh entry in the Star Wars film saga. It was also announced that Bryan Burk and Bad Robot Productions would produce the feature. Following the news that he would direct The Force Awakens, speculation arose as to Abrams’s future with Paramount Pictures, under which he had released all of his previous feature work as a director, and which had a first-look deal with his company, Bad Robot Productions. Paramount vice-chairman Rob Moore stated that Abrams would continue to have a hand in the Star Trek and Mission: Impossible franchises going forward.

On September 9, 2013, it was announced that Abrams would release a novel, S., written by Doug Dorst. The book was released on October 29, 2013.

Abrams directed, produced, and co-wrote the screenplay for The Force Awakens, which opened in theaters on December 18, 2015, and grossed over $2 billion at the box office, making Abrams the first director of a $2 billion movie since James Cameron. Despite its strong box office performance and positive reviews, the film was considered by some, including Star Wars creator George Lucas, to be too similar to the original 1977 film. In 2016, Abrams responded towards these complaints, stating: “What was important for me was introducing brand new characters using relationships that were embracing the history that we know to tell a story that is new — to go backwards to go forwards”.

In November 2015, it was announced that Abrams was developing video game called Spyjinx, in a collaboration between Bad Robot Productions And Chair Entertainment.

Abrams returned as producer for Star Trek Beyond, released in 2016. And also produced The Cloverfield Paradox, a sequel to 10 Cloverfield Lane. It was released on Netflix in February 2018. Also on 2018, Abrams produced Overlord, a horror film set behind German enemy lines in World War II and directed by Julius Avery. Abrams also produced the fourth, fifth, and sixth Mission: Impossible films.

In July 2016, Abrams reported that a fourth alternate universe Star Trek installment was in the works and that he is confident that Chris Pine, Zachary Quinto and Chris Hemsworth will return for the sequel.

In September 2017, it was announced by Lucasfilm’s president, Kathleen Kennedy, that Abrams would be returning to direct and co-write Star Wars: The Rise of Skywalker with Chris Terrio. The film was released in December 2019; it received mixed reviews from critics and fans, while audience reactions leaned more positively.

In February 2018, HBO ordered Abrams’ sci-fi drama Demimonde to series.

In May 2018, Abrams and Avery had reunited to produce and direct, respectively, a superhero thriller film titled The Heavy, with a script written by Daniel Casey. Paramount and Bad Robot plan to begin filming sometime in 2018.

In September 2019, Abrams and his Bad Robot Productions company signed a $250 million five-year deal with WarnerMedia, including HBO and Warner Bros. Pictures. In April 2020, it was announced that Abrams would be developing three new shows for HBO Max: Justice League Dark, Overlook, and Duster.

In 2019, Abrams made his debut as a writer for Marvel Comics, co-authoring the company’s title Spider-Man from September of that year with his son Henry. The first issue of the comic includes the death of Mary-Jane Watson, and a twelve-year time shift, with the series’ protagonist being Ben Parker, son of Peter Parker and Mary Jane.