The League of Gentlemen initially began as a stage act in 1995, transferred to BBC Radio 4 as On the Town with The League of Gentlemen in 1997 and then arrived on television on BBC Two in 1999. The latter saw Shearsmith and his colleagues awarded a British Academy Television Award, a Royal Television Society Award and the prestigious Golden Rose of Montreaux.
From March 2006 to January 2007, he appeared in the West End as Leo Bloom in The Producers.
Psychoville began June 2009 and marked his return to BBC2. The dark comedy series was written by Shearsmith and his League of Gentlemen writing partner Steve Pemberton. Both Shearsmith and Pemberton played numerous characters in the programme, which ran for two series and a Halloween special.
In 2010 Shearsmith appeared in John Landis' black comedy Burke and Hare and played the lead character in Ghost Stories, written and directed by Jeremy Dyson and Magician Andy Nyman.
In 2011, Cameron Mackintosh's new musical Betty Blue Eyes opened in the West End, in which Shearsmith played downtrodden husband Gilbert Chilvers (a chiropodist) alongside Sarah Lancashire. Also in 2011, he played Harry Wiseman in Eric & Ernie, a feature-length TV drama about Morecambe and Wise.
Also in 2013, he starred in Ben Wheatley's A Field In England as Whitehead and appeared in The World's End.
Also in 2014, he starred as Malcolm Webster in ITV drama series, based on a true story, The Widower. Also in 2014, he starred as Detective Sergeant Stone in Chasing Shadows, an ITV drama series about missing persons.
In 2015, he played Gagan Rassmussen in the Series 9 Doctor Who episode "Sleep No More", Steele in High-Rise directed by Ben Wheatley, Ray in Peter Kay's Car Share, and Pastor John in the Christmas specials of Julia Davis's Hunderby. In February 2015, Shearsmith was interviewed by Adam Buxton on BBC Radio 4's Chain Reaction and he then interviewed Bob Mortimer. Also in 2015, he appeared in Hangmen at the Royal Court Theatre from Thursday 10 September to Saturday 10 October 2015. The play was written by Martin McDonagh and directed by Matthew Dunster.
A Christmas special of Inside No. 9 aired in December 2016 and a third series aired in 2017.
In 2017, he appeared in the title role in The Dresser at Chichester Festival Theatre, as well as reuniting with The League of Gentlemen for three television specials, transmitted on BBC2 in December 2017.
