Jupitus worked in Essex at the Manpower Services Commission, part of the Department of Employment, for five years, while he also wrote political poetry and drew cartoons. He resigned from the department in 1984, hoping for a career in the music industry.

His performances of two of his poems, “Beano” and “Nobby”, were included in the 1986 album Not Just Mandela, alongside tracks by Billy Bragg and Attila the Stockbroker, amongst others. Released on Davy Lamp Records, all proceeds of the record were going to the Anti-Apartheid Movement.

Jupitus became press officer and compère for The Housemartins (appearing in the 1986 music video for “Happy Hour”), using the role to continue being in front of an audience, while also filling support slots for other artists. During this time, he worked as a warm-up act on the Channel 4 TV show The Show. He quit working for Go! Discs in 1989 and fell back on his poetry and competing to try and gain a foothold on the London comedy circuit.

Using the moniker Porky the Poet, Jupitus became associated with Anti-Fascist Action and the ranting poetry scene, alongside Kool Knotes, Seething Wells, Swift Nick and Attila the Stockbroker. Jupitus approached local bands to offer himself as a support act for their tours: “I thought it looked easy, I was very cheap. If you got another band to support you, there are probably four of them and roadies and managers. But me—I just turned up and read poems.” His first vinyl recordings were part of the live Newtown Neurotics album Kickstarting a Backfiring Nation as Porky the Poet in 1987.

He conceived and directed the Brit Awards-nominated music video for Bragg’s “Sexuality” in 1991 and wrote a parody version of that song about bestiality. He also appeared alongside R.E.M. in the music video for Bragg’s “You Woke Up My Neighbourhood” and performed in Searchlight magazine’s 2006 “Hope Not Hate” campaign tour with Bragg. He has also appeared numerous times at the Glastonbury Festival as a DJ and a compere in The Left Field tent. Jupitus produced the music video for Kirsty MacColl’s 1991 single “All I Ever Wanted” from the album Electric Landlady. He appeared at her tribute concert in 2002 as compere, and also sang one of her songs, “Fifteen Minutes”.

Jupitus was one of the panellists on the first TV episode of the show Loose Talk, which made a brief transition from radio to television in 1994. In 1996, he joined BBC Two’s pop quiz show Never Mind the Buzzcocks as a regular team captain – having appeared in every single episode, except for series 25, episode 6. He is the guest panellist who has made the most appearances on QI, while his daughter, Emily Jupitus, currently works on the show as a researcher (or ‘QI Elf’). He had a history of mimicking the QI host, Stephen Fry, while on the show. In December 1999, he had the lead role in Dark Ages, an ITV sitcom parodying preparations (and fears) for the year 2000, set in Essex in the year 999. Jupitus has played Councillor Cowdrey in CITV children’s series Bottom Knocker Street since its first series in summer 2013.

Jupitus began hosting his own radio show on BBC GLR in 1995, a regular job that would last until 2000. After that, he embarked on his first stand-up comedy tour of the UK, Jedi, Steady, Go, performing the Star Wars story in a comedic fashion.

In 2000, he released the stand-up comedy DVD Phill Jupitus Live: Quadrophobia. In 2001, he appeared as a sports journalist in the film Mike Bassett: England Manager.

In 2002, Phill Jupitus was a stand-in presenter on BBC Radio 2 for Steve Wright while he was away on holiday.

Jupitus made a guest appearance on the Bonzo Dog Doo-Dah Band 40th anniversary DVD performing with the band on the track “Mr. Apollo” and has toured with them around the UK. He appears on the Bonzos’ 2007 album, Pour l’Amour des Chiens. Also in 2007, he performed with The Blockheads on their 30th anniversary tour. He continued to perform with them sporadically since Ian Dury’s death, also appearing in Dury’s place for “Drip Fed Fred” during the Madness concert at Wembley Arena shortly before Dury’s death. Jupitus performed at the Reading and Leeds Festivals in 2008.

Jupitus co-wrote and starred in the play Waiting for Alice with Andre Vincent which had a run at the Edinburgh Fringe Festival. The world premiere took place on 16 July 2007 at the St. Ives Theatre in St Ives, Cornwall.

During the 2008 Major League Baseball season, Jupitus presented a feature during the seventh inning stretch of Channel Five’s featured Sunday night game. Each week he would read a section or quote from one of his favourite baseball-related books. He is a fan of the Boston Red Sox and has their logo tattooed on his arm.

In December 2008, Jupitus took part as a guest presenter on RTÉ’s comical topical discussion show The Panel.

From August 2008 he was the host of The Times football podcast “The Game”, replacing the previous co-hosts Gabriele Marcotti and Guillem Balagué, although Marcotti was still a regular pundit on the show and hosted again on Jupitus’ departure.

Between September 2008 and June 2011, Jupitus produced a podcast along with Phil Wilding, who produced his BBC 6Music show, called Phill and Phil’s Perfect Ten. Initially being released fortnightly, it later became more sporadic due to the pair’s work commitments. In April 2009, archive episodes were made available for purchase on Audible and iTunes as audiobook bundles of four with bonus ‘perfect ones’ attached. Since ending the podcast in June 2011 the pair have indicated that all back-episodes will be released free at some point in the future.

On 13–14 February 2009, Jupitus co-hosted the first BadMovieClub on Twitter. At midnight, over 2,000 Twitter users simultaneously pressed ‘Play’ on the film The Happening and continued to tweet whilst watching, creating a collective viewing experience that generated 40,000 tweets in under two hours. The first showing took place at 9:00pm, hosted by Graham Linehan. Jupitus was awarded an honorary doctorate by the University of Essex in South Essex College’s congregation ceremony in Southend on 30 September 2010. Jupitus was also awarded an honorary doctorate from the University of Kent, Canterbury in 2017, where his daughters had previously attended.

On 9 September 2009, Jupitus narrated a half-hour documentary on BBC Radio 4 about the comic strip Calvin and Hobbes created by Bill Watterson.

Jupitus and Marcus Brigstocke appeared together in the UK tour of Totally Looped, performing at the Theatre Royal, Brighton, the Kings Theatre, Southsea and the Victoria Hall, Stoke-on-Trent in spring 2009.

In October 2009, Jupitus joined the West End theatre cast of Hairspray, playing the role of Edna Turnblad at the Shaftesbury Theatre. He joined the 2011 tour of Spamalot, playing the role of King Arthur.

On 6 October 2010, Jupitus, along with Emma Kennedy, hosted a special comedy evening at the Canterbury Animation Festival ‘Anifest’.

Jupitus was the breakfast DJ on BBC Radio 6 Music from 2002 until 30 March 2007 (the last song played, by listener request, was “Broadway” by The Clash), and made brief returns to the station during the summer of 2007, sitting in for Stephen Merchant on Sunday afternoon and Liz Kershaw on Saturday mornings. In 2010, he publicly criticised the BBC’s announcement that it was to discontinue the station, describing the decision as “not only an act of cultural vandalism, it’s also an affront to the memory of John Peel and a slap in the face to thousands of licence-payers.” Jupitus has since written a book about his time on 6 Music, entitled Good Morning Nantwich: Adventures in Breakfast Radio. In February 2010, as part of his research for the book, Jupitus presented the breakfast show for one week on Bournemouth University student radio station, Nerve Radio, produced by Mog McIntyre and co-presented by regular student presenters ‘Guy Larsen & Jess Bracey’.

Jupitus discussed his arachnophobia with the writer and broadcaster Suzy Klein on the BBC Radio 4 programme I’m Suzy, and I’m a Phobic, which was broadcast in January 2013.

Jupitus attended the “I Do To Equal Marriage” event which celebrated the introduction of same-sex marriage in England and Wales in March 2014.

On 16 January 2015, Jupitus was confirmed as starring opposite Jason Manford in the 2015 tour of Mel Brooks’ musical The Producers, portraying Franz Liebkind. He has since appeared in Chitty Chitty Bang Bang also alongside Jason Manford on a tour of the UK.

In 2018 Jupitus was interviewed by Jodie Cook for the Clever Tykes podcast: Creating Useful People. The podcast explores the childhood influences that shape future success. In Jupitus’ episode he talked about how he developed his ethos for life and work, as well as his mum’s dreams for him as a naval merchant.

Jupitus has worked on Radio 4 as a regular contributor to Loose Ends, The News Quiz (where his performances are notable for a range of parody voices), I’m Sorry I Haven’t a Clue and Just a Minute. He also presented Best Sellers—a series on the life and work of Peter Sellers—and wrote and presented Disneyfied, a documentary on the work of Walt Disney. On 7 June 2020 he presented Pick of the Week.