He made his directorial debut with the neo-noir mystery film Brick (2005), which received positive reviews and grossed nearly $4 million on a $450,000 budget.

Transitioning to higher-profile films, Johnson achieved mainstream recognition for writing and directing the science-fiction thriller Looper (2012) to critical and commercial success.

Johnson landed his largest project when he wrote and directed the space opera Star Wars: The Last Jedi (2017), which grossed over $1 billion.

!, loosely based on Edgar Allan Poe's "The Tell-Tale Heart", was included as an easter egg on the Looper Blu-ray.

He is a professed fan[citation needed] of the band and was asked to direct the video when bandleader John Darnielle noticed a reference to them in the credits for Brick.

The film consists of a single shot, depicting Darnielle performing the entire album on guitar and piano with minimal accompaniment.

This film was screened in New York City, Chicago, Seattle, and Portland, Oregon upon its completion, and was released as a limited edition DVD on Record Store Day (April 17, 2010).

[23] Johnson confirmed the report that following month and the film, Star Wars: The Last Jedi, was released on December 15, 2017, to positive reviews from critics and audiences.

[24] After Colin Trevorrow departed Episode IX, Johnson turned down an offer from Lucasfilm to write and direct the follow-up to The Last Jedi.

[26] Following The Last Jedi, Johnson directed the murder mystery film Knives Out, starring Daniel Craig, Ana de Armas and Christopher Plummer.

[29][30] In September 2019, Johnson and producer Ram Bergman launched T-Street, a company that will generate original content for film and TV shows.

[31] Due to the success of Knives Out, Lionsgate announced that a sequel was officially approved in February 2020, with Johnson set to return to write and direct the film.

[32] In March 2021, it was announced that Johnson was writing/directing a ten-episode mystery drama television series for Peacock titled Poker Face, starring Natasha Lyonne, which premiered on the service on January 26, 2023.