He achieved early success with roles in the films Hackers (1995) and Trainspotting (1996), and worked steadily in film and theatre until 2008, when he starred as the series lead in two seasons of the American television series Eli Stone. He followed this up with lead roles in the Broadway play After Miss Julie and the BBC production of Emma. In February 2011, he starred in Danny Boyle's stage adaptation of Mary Shelley's Frankenstein opposite Benedict Cumberbatch.

Miller was born in Kingston upon Thames, London, England, the son of Anne Lee, who worked in theatre production and starred in many films (including Lost & Found), and Alan Miller, a stage actor and later a stage manager at the BBC.

His maternal grandfather was actor Bernard Lee, famous for playing the character M in the first eleven James Bond films. Miller has stated that he has fond memories of being at the BBC Television Centre with his sister and watching Top of the Pops and Blue Peter being made.

He made an uncredited appearance in the BBC series Doctor Who as a child in the 1982 story Kinda. Miller was educated at Tiffin School in Kingston upon Thames where he gained his first acting experience (notably in the musical The Ragged Child, written by the school's Director of Music David Nield, and Head of Drama Frank Whately) and played in the Tiffin Swing Band. Miller left school at age 17 to pursue his acting career.

After a stint in EastEnders as Jonathan Hewitt, Miller got his big break in the film Hackers (1995), co-starring with Angelina Jolie, whom he married in 1996. In 1997, Miller was involved with the creation and operation of Natural Nylon along with friends Jude Law (whom he met in the National Youth Music Theatre), Sadie Frost, Ewan McGregor, Sean Pertwee, Damon Bryant, and Bradley Adams. Natural Nylon folded in 2003. Aside from EastEnders, he has appeared on television in the BBC's modernisation of The Canterbury Tales, as Artie in The Pardoner's Tale and as Lord Byron in a BBC production about the life of the poet. He worked on the US television series Smith in 2006. His first appearance on US television was the 1996 miniseries Dead Man's Walk.

Shortly after Hackers, he was cast in Trainspotting as "Sick Boy". He was suggested for that role by Ewan McGregor. The accent he used in the film was so convincing that it led many people[citation needed] to erroneously believe he was from Scotland. It states on Miller's website, "As the only non-Scot in the cast Jonny has had to master the accent. "I had to do a lot of work," he confesses, "I read and re-read the book and I pretended to be Scottish all the time I was in Glasgow, hanging around with Scots, picking up bits and pieces on the street and in bars. Everyone's been very encouraging and Danny thinks that I've got it about right. Of course, the others are from all over Scotland and have different accents themselves, so I've tried to just pick up a general, composite accent."

In 1997, he played Billy Prior in the film adaptation of Pat Barker's World War I novel, Regeneration. In 2000, he played the role of Cameron Colley in Complicity, based on the book by Iain Banks. He costarred alongside Jude Law and Ray Winstone in the film Love, Honour and Obey as Johnny, a London street kid getting mixed up with a notorious Brit gangster.

Also in 2000, he appeared as Simon Sheppard in Wes Craven's Dracula 2000. In 2005, he was considered for the role of James Bond, to replace Pierce Brosnan. The role went to Daniel Craig. The following year, Miller portrayed cyclist Graeme Obree in The Flying Scotsman. In 2007, he was selected to play the lead role in the series for ABC, called Eli Stone; the series was canceled after two seasons. The first season had been interrupted by a lengthy writers' strike.

He was considered as the third teammate to join Ben Fogle and James Cracknell in Team QinetiQ for the Amundsen Omega 3 South Pole Race (January 2009). He participated in training for the event in Norway which was televised for a BBC2 documentary series On Thin Ice. He was not able to attend the race due to filming commitments of Eli Stone being extended for a second season. In 2009, he played Mr. Knightley in a BBC adaptation of Jane Austen's Emma.

He also appeared on Broadway with Sienna Miller in a production of "After Miss Julie", his performance receiving generally excellent reviews. In early 2010, Miller was apparently in talks to portray Rick Grimes in the TV adaptation of the comic The Walking Dead, but the part went to Andrew Lincoln. Miller starred in the fifth season of Dexter as Jordan Chase, a highly popular motivational speaker who is suspected of leading a gang of serial rapists and murderers.

In March 2011, at the Royal National Theatre, he played, on alternate nights, both Victor Frankenstein and his Creature, opposite Benedict Cumberbatch, in a stage adaptation of Frankenstein.

Frankenstein, directed by Danny Boyle, was broadcast to cinemas worldwide as part of National Theatre Live on 17 March 2011 and additional dates throughout March and April.

He appeared in Tim Burton's film Dark Shadows (2012). In February 2012, it was confirmed Miller had been cast as Sherlock Holmes in the CBS drama Elementary. Lucy Liu was later cast as Watson.

Miller is a supporter of Chelsea Football Club. He is a marathon runner, often supporting the charity Mencap. Miller was signed up to run their 2006 Marathon des Sables but had to drop out due to filming the movie Marathon. He ran the 2008 London Marathon in 3:01:40.

He ran the 2010 New York City Marathon with his Dexter co-star Jennifer Carpenter.

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