He is best known for playing Dennis Reynolds on the long-running sitcom It's Always Sunny in Philadelphia (2005–present) on FX/FXX, a series he co-developed[1] with Rob McElhenney, and on which he serves as an executive producer and writer.

[3] His other notable performances on television include Corey Howard in That '80s Show (2002), Cliff Gilbert on Fox's The Mindy Project (2012–2017), Don Chumph on the first season of FX's Fargo (2014) and Jack Griffin, the lead role on NBC's A.P.

Howerton is most well known for playing the deeply narcissistic and anti-social bartender of Paddy's Pub, Dennis Reynolds, one of the main characters on the FX sitcom It's Always Sunny in Philadelphia (2005–present).

The series was co-created by Rob McElhenney, Charlie Day and him, and the three serve as executive producers, writers and main cast members alongside Kaitlin Olson and Danny DeVito.

[13] Howerton also played a small part as the gun-running Dominic in the Netflix Original film Officer Downe (2016) starring Kim Coates.

Bio (2018–2021), where he played Jack Griffin, an arrogant Harvard philosophy professor whose fall from grace had forced him to get a job teaching biology to high school students in his hometown of Toledo while plotting to exact revenge on his nemesis and restore his career.

[19][20] In August 2022, after production had wrapped, it was announced that Howerton would be co-starring with Jay Baruchel in a Canadian biopic directed by Matt Johnson on the rise and fall of BlackBerry as one of its co-founders.

[21] The film BlackBerry (2023) premiered in competition at Berlinale 2023 on February 17 to positive reviews from critics with Howerton's performance as Jim Balsillie being especially well received.

[22][23][24] In July 2024, it was announced that Howerton would be playing Ethan Corbin II, a lifelong bachelor burning through his trust fund, on the upcoming Netflix dark comedy limited series Sirens.