Film and television
Between 1998 and 1999, Berry appeared in the video game magazine show Game Over on BSkyB's computer and technology channel .tv.
Berry appeared in a UK television commercial for Lloyds TSB bank with singer Lionel Richie.
Berry's first prominent television role was Todd Rivers/Lucien Sanchez in the cult 2004 comedy series Garth Marenghi's Darkplace and its 2006 spin-off, Man to Man with Dean Learner. He later appeared as eccentric, sinister tycoon Dixon Bainbridge in The Mighty Boosh. He met the show's Julian Barratt and Noel Fielding while performing at the Hen and Chickens Theatre, where they were resident in 2000. He can be seen in a cameo performance in The Mighty Boosh Live DVD.
After meeting Rich Fulcher while filming The Mighty Boosh, Berry co-created, co-wrote, and co-starred in the comedy series Snuff Box with him on BBC Three; Berry also composed the main theme song and score for the series. Fulcher had co-starred as Bainbridge's lackey Bob Fossil in The Mighty Boosh. Berry also starred with Fulcher and Simon Farnaby on E4's The Golf War in November 2007.
In 2007, Berry joined The IT Crowd during its second series as Douglas Reynholm. He was nominated as Best Male Comedy Newcomer in the 2007 British Comedy Awards for the role.
In 2008, he became the face of Adult Swim's spoof charity appeal "Save the Workers".
In 2010, Berry played journalist Michael Duffy in the BBC production Five Daughters, about events surrounding the Ipswich murders of 2006. In 2011, he provided the voice of Allen in the Aqua Teen Hunger Force episode "Allen Part Two". He appeared in the British comedy panel game Shooting Stars, portraying Vangelis. He appeared as an antiques expert in the ITV sketch show Monkey Trousers with Vic and Bob and Steve Coogan.
Berry appeared in a number of films during this period, including The Devil's Chair (2006) and Moon (2009). He starred in The Search (2009), a short film about "a lonely man's search for the existence of life outside our universe takes a remarkable turn when he connects with a recently bereaved family".
In 2012, BBC Radio 4 aired his comedy series I, Regress, where he portrayed Dr. Berry, a brilliant but unorthodox regressive therapist. In each 15-minute episode, Berry explored the psyche of a guest patient, attempting to treat their problems in surreal dreamlike sequences. Berry appeared in the film adaptation of the David Nicholls novel One Day as Aaron, Dexter's agent. He was briefly featured in the closing ceremony of the 2012 Summer Olympics in London, introducing ELO's "Mr. Blue Sky" by way of a mock weather forecast.
In July 2012, he appeared as vainglorious actor Steven Toast in the pilot episode of Channel 4 sitcom Toast of London, co-written with Arthur Mathews. Notwithstanding mixed reviews, a series was commissioned, and the first episode was broadcast on 20 October 2013, and it brought Berry the 2015 BAFTA Award for Best Male Comedy Performance. In 2015, Berry and Arthur Mathews published Toast on Toast: Cautionary Tales and Candid Advice, a spoof autobiography of Steven Toast. It was released as an audiobook read by Berry.
Berry played the title character in the 2013 Portlandia episode "Squiggleman". Co-creators Fred Armisen and Carrie Brownstein included the appearance on a list of their "proudest musical moments" from the show.
From 2014 to 2015, Berry co-starred in the BBC 2 series House of Fools, written by and starring Reeves and Mortimer. He portrayed Beef, "the highly sexual, flamboyant and blindly confident friend of Vic and Bob" who "will seduce anything in a skirt".
Berry appeared in episode nine of the sixth season of Dan Harmon's television series Community, released on Yahoo Screen on 5 May 2015. In December 2015, he played Professor Awfulshirt in Harry Hill in Professor Branestawm Returns on BBC One.
Since 2019, Berry has starred in the FX TV adaptation of the film What We Do in the Shadows as Laszlo, one of four vampires living in Staten Island. It was renewed for a second season in May 2019, and began airing in April 2020. The third season aired in September 2021. In an interview with collider.com, Berry said, "It's different and it's very free. The scripts are starting points and then we go from there. That's how I like to work, anyway. So, for me, it was perfect. That's my background, improvisation. It was home for me in that department."
In 2019, Berry starred in the IFC/Channel 4 sitcom Year of the Rabbit. Set in Victorian London, he plays the alcoholic Detective Inspector Rabbit. On 11 February 2020, the series was renewed for a second series of six episodes. Citing budget cuts caused by the COVID-19 pandemic, Channel 4 reversed their decision in January 2021, casting doubt on the show's future. Layla Smith, chief executive of the show's production company OMG, said "Year of the Rabbit is a victim of the devastating effects of COVID. [...] IFC are very committed to the show, but we will need to find another partner — and we're working on that."
In April 2020, BBC Two commissioned Berry for a mockumentary series titled Squeamish About ... The four quarter-hour specials would be cowritten by Berry and Arthur Mathews and star Berry as Michael Squeamish. The series uses a combination of archive footage and voiceover to produce a surreal perspective on the episodes' subject.
In 2021, after the second series of Year of the Rabbit was axed, Berry was commissioned by the BBC to make a "Steven Toast in America" series. The show was a six-part television programme for BBC One, broadcast under the title Toast of Tinseltown and co-written by Berry and Arthur Mathews.
In September 2024, Deadline announced that Berry and Natasha Lyonne are creating and starring in a "retro series for Sky titled Force & Majeure."
In March of 2026, Berry was the announcer for the 98th Academy Awards.