As an actor, Heidecker's filmography includes roles in Bridesmaids (2011), Tim and Eric's Billion Dollar Movie (2012), The Comedy (2012), Ant-Man and the Wasp (2018), and Us (2019).

[4] Heidecker and Wareheim created, wrote, and starred in Tom Goes to the Mayor, a limited animation series that aired from November 2004 to September 2006 on Adult Swim.

According to their website, Wareheim and Heidecker had mailed copies of an early version of the show to comedian Bob Odenkirk, who agreed to take on the project as the executive producer of the series and sold it to Adult Swim.

They also created and starred in Tim and Eric's Billion Dollar Movie, and appeared together as debt collectors on the Adult Swim special Young Person's Guide to History and have made guest appearances in the movie Let's Go to Prison, as well as the Scottish video game series VideoGaiden and a Version 2 episode of Mega64.

[7] In the same year, Heidecker made a cameo appearance on the independent movie reviewing site, Red Letter Media.

Since 2012, Heidecker has hosted a parodic web series and podcast called On Cinema, where he and special guest (Gregg Turkington) discuss films from past and present.

Heidecker, Wareheim, Sarah Silverman, Michael Cera, and Reggie Watts announced on the podcast Comedy Bang!

Since 2016, Heidecker has hosted the podcast and web series Office Hours Live along with Vic Berger and Doug Lussenhop.

[9] The duo's anthology horror series, Tim and Eric's Bedtime Stories, aired on Adult Swim from 2014 to 2017.

In 2013, Heidecker released the album Urinal St. Station under the Drag City label with his band, The Yellow River Boys.

[20] In August 2020, Heidecker announced Fear of Death, a concept album featuring members of Foxygen, The Lemon Twigs, and Weyes Blood, slated for release on September 25 from Spacebomb Records.

[21] Heidecker's sixth album, High School, was released June 24, 2022, on Spacebomb Records[22] followed by a supporting North American tour.