2010–present: The Invitation, XX, and Destroyer
In 2013, Kusama directed the short film Speechless. Starting in 2014, Kusama began working regularly in television as a director on several series, such as Halt and Catch Fire, The Man in the High Castle, Casual, Billions, and The Outsider. Kusama was slated to direct an adaptation of Breed, an adult horror novel by Scott Spencer under the pen name Chase Novak. The film was to be produced and written by Kusama's husband Phil Hay and his partner Matt Manfredi, but there have been no updates since the film's announcement.
In 2015, Kusama directed The Invitation, a horror film written by Hay and Manfredi, and starring Logan Marshall-Green. The film was funded by a film consortium called Gamechanger Films, who fund films directed by women. It premiered at the 2015 SXSW Festival, to great acclaim, and was released by Drafthouse Films. The film would win the International Critic's Award at the 2015 Neuchâtel International Fantastic Film Festival, and was also nominated for Best Picture. Other accolades won by the film included Best Film at the 2015 Sitges Film Festival and the Golden Octopus at the 2015 Strasbourg European Fantastic Film Festival.
Part of the film's inspiration were the experiences of loss that Kusama, Hay, and Manfredi had. Kusama's brother, Kevin, died when she was young, as did a close friend in New York. The film was shot in sequence, cost US$1 million and was filmed in 20 days in Los Angeles. Due to the low production cost and time of the film, Kusama noted that despite the challenges involved with making a film in this manner she had the creative control she lacked on her previous Hollywood films.
In 2017, Kusama wrote and directed a segment, titled "Her Only Living Son", in the all-female directed anthology horror film XX. In 2018, Kusama directed the crime drama film Destroyer, which starred Nicole Kidman and Tatiana Maslany. According to Kusama, Kidman had lobbied for the part after reading the script. The film made its debut at the Telluride Film Festival to positive reactions for Kusama's direction and Kidman's performance, but disappointed at the box office, grossing slightly over $5 million globally with a budget of over $10 million.
In 2020, a new Dracula film was announced as in development by Blumhouse Productions, featuring Kusama as director and Phil Hay and Matt Manfredi as writers. The film was to be set in modern times and follow the character Mina Harker; however, the film was canceled in April 2022, just three weeks before it was to start filming.
In October 2024, Kusama was announced as the director and executive producer for a potential limited series based upon R. F. Kuang's 2023 novel Yellowface that had been optioned by Lionsgate Television.