Fukunaga originally wanted to be a pro Snowboarder, but switched to filmmaking in his mid-twenties. He got his start as a camera intern and later applied to film school. He graduated from the University of California, Santa Cruz with a Bachelor of Arts in history in 1999, and attended Institut d'études politiques (IEP) de Grenoble. He enrolled in New York University's Tisch School of the Arts Graduate Film Program.

Through his production company, Parliament of Owls, Fukunaga has produced or served as executive Producer on most of the projects he has directed. He was the executive Producer for his short films Kofi (2003) and Victoria para chino (2004). He was an executive Producer on Andrew Okpeaha MacLean's feature film thriller, On the Ice, which won "Best Debut Film" and the "Crystal Bear" (Best Feature Film for the Generation 14+) at the 2011 Berlin Film Festival, among other awards.

Fukunaga wrote and directed the short film Victoria para Chino (2004) while at NYU, which screened at the Sundance Film Festival and received a Student Academy Award in 2005. The film won an Audience Award for Best Narrative Student Short film at the 2004 Austin Film Festival, a "Best Student Film" award at the 2006 Ashland Independent Film Festival, a "BAFTA/LA Award for Excellence – Honorable Mention" award at the 2005 Aspen Shortsfest, Best Student Film at the 2005 BendFilm Festival, Best Short Film and an Audience Award for Best Short Film at the 2005 Gen Art Film Festival, Best Short film at the 2005 Milan International Film Festival, and the Jury Prize for Best Student Short at the 2004 Woodstock Film Festival.

He served as a camera operator on the short Glory at Sea (2008) (directed by Beasts of the Southern Wild Director Benh Zeitlin), as a gaffer on the short film Just Make Believe (2008) (directed by Jadrien Steele), as an additional Cinematographer on the TV documentary Small Steps: Creating the High School for Contemporary Arts (2007), assistant camera on the short film Dock (2004) (directed by Nina Martinek), additional photography for the documentary Lockdown, USA (about the "War on Drugs" campaign and directed by Rebecca Chaiklin and Michael Skolnik), additional camera for Autumn's Eyes (2006) (directed by Paola Mendoza and Gabriel Noble), a grip on the feature film Mango Kiss (2004) (directed by Sascha Rice), and as an additional film loader on the feature film Black Cadillac (2003) (directed by John Murlowski and starring Randy Quaid).

Fukunaga made his feature film debut with Sin Nombre, which he wrote and directed. It received positive reviews. The film received a number of awards, including the Directing award at the 2009 Sundance Film Festival and a "New Director's Award" for Fukunaga at the 2009 Edinburgh International Film Festival. I need 2009, the film won "Best Foreign Language Film" awards from the Austin Film Critics Association, the Dallas-Fort Worth Film Critics Association Awards, the Florida Film Critics Circle Awards, the San Diego Film Critics Society Awards (2nd place for Best Foreign Language Film), and the Washington DC Area Film Critics Association Awards. The film's Cinematographer, Adriano Goldman, won the Cinematography award at the 2009 Sundance Film Festival, and at the 2009 Stockholm Film Festival, the film won a Best Actor award (for Edgar Flores), as well as a Best Directorial Debut and FIPRESCI Prize for Fukunaga. Fukunaga won a 2010 Premios ACE award for "Cinema – Best First Work." The film was nominated for Best Feature, Best Director and Best Cinematography from the 2010 Independent Spirit Awards, and was nominated by the 2009 British Independent Film Awards (Best Foreign Film), the 2010 Broadcast Film Critics Association Awards (Best Foreign Language Film), the 2009 Chicago Film Critics Association Awards (Most Promising Filmmaker; Best Foreign Language Film), the 2010 Image Awards (Outstanding Foreign Motion Picture), the Bronze Horse at the 2009 Stockholm Film Festival and the 2009 Sundance Film Festival Grand Jury Prize.

In 2010, Fukunaga directed a new film adaptation of Jane Eyre starring Mia Wasikowska, Michael Fassbender, Jamie Bell and Judi Dench. The film was released in 2011 and was nominated for an Academy Award for Best Achievement in Costume Design for Costume Designer Michael O'Connor and a 2012 Goya Award for Best European Film. The film was nominated for a 2012 BAFTA Award (Best Costume Design), a 2012 Broadcast Film Critics Association Award (Best Costume Design), the 2012 Costume Designers Guild Awards (Excellence in Period Film), the 2012 Evening Standard British Film Awards (Best Technical Achievement), the 2011 Phoenix Film Critics Society Awards (Best Costume Design), the 2011 Satellite Awards (Best Costume Design). The 2012 Australian Film Institute awards as well as the 2011 British Independent Film Awards nominated Mia Wasikowska for a "Best Actress" award. The film's screenplay and Screenwriter Moira Buffini (as well as author Charlotte Bronte) were nominated for a 2012 USC Scripter Award.

Fukunaga served as a Cinematographer on a number of short film projects, including Handmade (2013) (a documentary short directed by Rob Meyer), Sikumi (2008) (also known as Sikumi (On the Ice) about an Inuit hunter on the frozen Arctic Ocean, directed by Andrew Okpeaha MacLean), Team Queen (2007) (a short film directed by Leah Meyerhoff), the feature documentary Death of Two Sons (2006) (directed by Micah Schaffer), the short films Clear Water (2005) (directed by Natalie Mooallem), White (2005) (directed by Sebastian Mantilla), Kinnaq Nigaqtuqtuaq (2005) (directed by Andrew Okpeaha MacLean), Two Men (2005) (directed by Ian Olds) and Mating Call (2004) (directed by Patricio Serna).

Fukunaga directed all eight episodes of the first season of the 2014 HBO TV series True Detective, which was written and created by Novelist, fiction Writer and Screenwriter Nic Pizzolatto. The series stars Matthew McConaughey, Woody Harrelson and Michelle Monaghan. Fukunaga served as an Executive Producer on the show. The series received critical praise and was nominated for five Primetime Emmy Awards, including Outstanding Drama Series and Outstanding Directing for Fukunaga, who won. For the second season of True Detective, Fukunaga did not return as Director, but continued to serve as executive Producer.

In April 2015, Deadline.com reported that Fukunaga was pairing again with Anonymous Content Productions to direct the TV series The Alienist , based upon the best selling novel of the same name by author Caleb Carr. The series is to be aired on TNT. In September 2016, Jakob Verbruggen replaced Fukunaga as Director due to scheduling conflicts, although he will retain "created by" credit and will remain an executive Producer.

In February 2017, it was reported Fukunaga was in talks to direct Shockwave, a drama about the lead-up to the dropping of the atomic bomb on Hiroshima.