During a road trip from Kansas to San Francisco, her mother dropped Jenkins and her sister off at a movie theater, where they watched the original Superman starring Christopher Reeve.

At age 20, while interning at a commercial production company, she heeded a suggestion that she could receive film training if she worked on set for free.

While shooting a Michael Jackson music video, her director of photography recommended that she attend the American Film Institute to learn directing.

There she met Brad Wyman, who later introduced her to producer Donald Kushner, leading to her directing her first feature film, Monster (2003).

Jenkins ended up writing to the film's subject, serial killer Aileen Wuornos, who was a street prostitute who went on a 1989–1990 murder spree of seven of her male clients, and was at the time on death row.

After the success of Monster, Jenkins was approached by former United States Air Force test pilot Chuck Yeager to develop a film about his life.

When that project did not reach fruition, she attempted to make a Ryan Gosling movie titled I Am Superman, a film with no relation to the DC Comics character, but development ended when she became pregnant.

[22] The film was released in June 2017, and gave Jenkins the biggest domestic opening for a female director, surpassing previous record holder Fifty Shades of Grey by Sam Taylor-Johnson.

[24][25] The film was acclaimed by both critics and audiences and grossed over $800 million worldwide, exceeding box office original predictions.

[28] In July 2017, the cable network TNT announced Jenkins would direct the premiere of a six-episode television drama, I Am the Night, written by her husband Sam Sheridan, and featuring her Wonder Woman star Chris Pine.

It had originally been scheduled for November 1, 2019;[33] unlike the first film, the sequel received a mixed critical reception and was a box office failure.

She has been negotiating the terms of her contract with Warner Brothers for an estimated seven to nine million dollars, which would be a record breaking salary for a female filmmaker.

The film will star Gadot as the titular Cleopatra, the historical pharaoh of ancient Egypt, with Jenkins as the director.

[35] In November 2020, a spin off film set in the Wonder Woman universe focusing on the Amazons of Themyscira was confirmed to be in early development.

[38] In December 2020, Disney announced that Jenkins was hired to direct Rogue Squadron, a Star Wars spin-off film inspired by the group of starfighter pilots of the same name.

[44] In March 2024, Jenkins revealed that following the cancellation of the third Wonder Woman film, she had returned to Rogue Squadron, finalizing a deal with Lucasfilm prior to the 2023 Writers Guild of America strike, and that she now "owes" a new draft of the script.

[45] Jenkins, Wonder Woman actresses Gal Gadot and Lynda Carter, DC Entertainment President Diane Nelson and U.N. Under-Secretary General Cristina Gallach appeared at the United Nations on October 21, 2016, the 75th anniversary of the first appearance of Wonder Woman, to mark the character's designation by the United Nations as its "Honorary Ambassador for the Empowerment of Women and Girls".

[46][47][48] The decision was met with protests from UN staff members who stated in their petition to UN Secretary-General Ban Ki-moon that the character is "not culturally encompassing or sensitive", and served to objectify women.

[54] She received two nominations at the 2012 Directors Guild of America Awards for Outstanding Directorial Achievement, one for Dramatic Series for The Killing and the other for Movies for Television/Mini-Series for Five; she won the former.