[5] In 2010, she directed City Lax: An Urban Lacrosse Story, making her debut in independent feature documentary-making.

The subject was chosen by her classmate Tor Myhren, and the documentary tells the story of Tor's brother Erik, who at the time was an elementary school teacher that put together a lacrosse team in a rough urban neighbourhood to play a rich white kids' sport.

[6] In 2013, Cowperthwaite directed her second documentary Blackfish, which premiered at the 2013 Sundance Film Festival, and found a larger audience on television via her distribution partner CNN.

Blackfish is a controversial documentary, as it tells the story of Tilikum, an orca at the SeaWorld theme park in Orlando, Florida who killed its trainer, Dawn Brancheau.

A drama based on real events, the film follows a corporal in the U.S. Marine's K9 unit, working with a German shepherd named Rex to detect explosives and weapons during the Iraq War.

[9] In 2019, Cowperthwaite directed Our Friend, a drama film starring Casey Affleck, Dakota Johnson, and Jason Segel, revolving around real-life couple Nicole and Matthew Teague.