He appeared in minor roles in films such as Naked (1993), Les Misérables (1998), Ever After (1998), Finding Neverland (2005), and Mrs Henderson Presents (2005).

He has since acted in Amazing Grace (2006), The Painted Veil (2006), W. (2008), Frost/Nixon (2008), Tinker Tailor Soldier Spy (2011), My Week with Marilyn (2011), Berberian Sound Studio (2012), Dad's Army (2016), Journey's End (2017), and Empire of Light (2022).

Jones is also known for his voice roles as Dobby in the Harry Potter films (2002–2010), Aristides Silk in The Adventures of Tintin (2011) and Owl in Disney's Christopher Robin (2018).

He is also known for his blockbuster roles as Claudius Templesmith in The Hunger Games franchise (2012–2013), Arnim Zola in the Marvel Cinematic Universe (MCU) films Captain America: The First Avenger (2011) and Captain America: The Winter Soldier (2014), Mr. Eversoll in Jurassic World: Fallen Kingdom (2018), and Basil Shaw in Indiana Jones and the Dial of Destiny (2023).

Jones's television credits include Doctor Who (2010), Julian Fellowes's Titanic miniseries (2012), MCU's Agent Carter (2015), Sherlock (2017) and What If...?

Jones appeared in the 2010 episode "Amy's Choice", of Doctor Who, as the Dream Lord, and in the Big Finish Productions series' Dark Eyes (audio drama) as Kotris.

He also played the role of Samuel Ratchett in Agatha Christie's Poirot TV Series 12 episode "Murder on the Orient Express".

In 2011, he played the role of the British spy master Percy Alleline in the adaptation of John Le Carré's Tinker Tailor Soldier Spy and Arnim Zola in Captain America: The First Avenger, a role which he reprised in the sequel Captain America: The Winter Soldier three years later as well as in a cameo in the TV series Agent Carter the following year.

In 2012, he had a leading role in the ITV mini-series Titanic, starred as one of the seven dwarves in Snow White and the Huntsman, played Dr. Paul Shackleton in Red Lights, and Max in Virginia.

[5][6][7][8][9][10] Sam Wollaston, in The Guardian, praised Jones's "lovely, very human, performance",[11] one that earned him his second British Academy Television Award nomination.

In 2015, Jones played the part of Roger Yount, a banker, in the three-part BBC series Capital based on John Lanchester's novel of the same name.

Since 2013 Jones has been the voice of the lead character, Joey Oldman in the BBC Radio 4 series The Corrupted, an adaptation of the G. F. Newman novel Crime and Punishment.

His comic turn as Arthur earned him the Olivier Award for Best Actor in a Supporting Role, and the play moved to Broadway in 2003.

[24] In 2020, he starred in the title role in the Conor McPherson adaptation of Uncle Vanya by Anton Chekhov, at the Harold Pinter Theatre.