In 2002, Howerton starred as Corey Howard in That ’80s Show. He went on to guest star on ER as Dr. Nick Cooper in 2003. He had small roles in the films Must Love Dogs (2005), Serenity (2005), Two Weeks (2006), and The Strangers (2008). He also appeared as a nurse in Crank (2006), and reprised the role in its 2009 sequel, Crank: High Voltage. Howerton is most notably involved in “It’s Always Sunny in Philadelphia” (2005-) as one of the main cast, producer and director, he also has written numerous episodes. He planned to be executive producing on the comedy show Boldly Going Nowhere with his It’s Always Sunny in Philadelphia co-creators, before the show was delayed. Howerton had a recurring voice role on The Cleveland Show as Ernie Krinklesac, as well as recurring roles on the Fox comedy series The Mindy Project and the FX dark comedy series Fargo. He starred in the 2013 comedy film Coffee Town. He also had a bit part as the gun running Dominic, in the recently released Netflix Original Officer Downe, starring Kim Coates.
Howerton was born in Japan, the son of American couple Janice and Glenn Franklin Howerton Jr., a fighter pilot. He grew up in London and South Korea. When he was 10 years old, his family moved to Alabama. After graduating from Jefferson Davis High School in Montgomery, Alabama, he spent two years at New World School of the Arts in Miami, Florida. He was part of Group 29 of the Juilliard School’s Drama Division (1996–2000), where he graduated with a Bachelor of Fine Arts.