Hawley graduated from Sarah Lawrence College with a degree in political science in 1989. He worked for Legal Aid Society in New York City, dealing with cases involving child abuse and neglect. He later moved to San Francisco and did computer programming work at law firms and worked as a paralegal.
He has published five novels: A Conspiracy of Tall Men (1998), Other People's Weddings (2004), The Punch (2008), The Good Father (2012), and Before the Fall (2016).
Hawley was a Writer and Producer on the first three seasons of the television series Bones (2005–2008). He was also creator and executive Producer of The Unusuals (2009) and My Generation (2010).
Hawley wrote the original screenplay for the film The Alibi (2006).
In September 2014, it was announced that Hawley had signed a deal with Universal Pictures to script an untitled project for their upcoming Dark Universe. Sony Pictures has acquired the rights to Hawley's latest novel, Before the Fall, with him writing the screenplay.
In December 2015, Hawley extended his production deal with FX. He wrote and served as executive Producer for Legion, an FX television series based on the Marvel comic book character. Hawley will also write and executive produce a limited series adaptation of Kurt Vonnegut's Cat's Cradle for FX. He will executive produce, but not write for, two additional adaptations for FX: Hellhound On His Trail, based on the book of the same name, and The Hot Rock, also based on a book.
Hawley will make his feature film directorial debut with Pale Blue Dot, a sci-fi film with Natalie Portman as an Astronaut for Fox Searchlight. He has also been set to direct Man Alive, from a sci-fi spec script by first-time Screenwriter Joe Greenberg. On July 20, 2017, Hawley announced at Comic Con that he is writing and directing a Doctor Doom movie with 20th Century Fox.