After National Service in the Army (part of which he spent as an announcer and drama Director with the British Forces Broadcasting Service) he obtained a place at the College of Dramatic Arts in Glasgow. After a period at the Old Rep (also known as the Birmingham Repertory Theatre), he appeared with the Royal Shakespeare Company (RSC), of which he was a founding member, from 1960 to 1975.

In 1963, he played Le Beau in Michael Elliott's television production of As You Like It, playing alongside Vanessa Redgrave. In 1964, he played Antipholus of Ephesus in The Comedy of Errors as part of the Festival television series. In 1966, he played Jean-Paul Marat in the Royal Shakespeare Company production of Peter Weiss' Marat/Sade, directed by Peter Brook. In 1967, he played The Constable in A Man Takes a Drink as part of a television series entitled The Revenue Men. He played Bertram in John Barton's television version of All's Well That Ends Well in 1968, as well as playing Oberon in the Peter Hall film of A Midsummer Night's Dream. He took part in the television production of John Mortimer's A Voyage Round My Father in Plays of Today in 1969 as well as appeared in the television adaptation of The Canterbury Tales (1969).

While at the RSC, Richardson played leading roles in many productions for Director John Barton. These included the title role in Coriolanus (1967), Cassius in Julius Caesar (1968), Angelo in Measure for Measure (1970) and Iachimo in Cymbeline. Work for other Directors at Stratford included the title role in Pericles (1969), directed by Terry Hands; the title role in Richard III (1975), directed by Barry Kyle; and Berowne in David Jones' production of Love's Labour's Lost (1973). Richardson cited the role of Berowne as one of his all-time favorite parts. Richardson's Richard II (alternating the parts of the king and Bolingbroke with Richard Pasco) in 1974, and repeated in New York and London in the following year, was hugely celebrated:

A significant Shakespearean cameo role was a brief performance as Hamlet in the gravedigger scene as part of episode six, "Protest and Communication", of Kenneth Clark's Civilisation television series in 1969. This was performed at Kirby Hall in Northamptonshire with Patrick Stewart as Horatio and Ronald Lacey as the gravedigger.

In 1972, he appeared in the musical Trelawney, with which the Bristol Old Vic reopened after its refurbishment. It proved a great success, transferring to London, first to the Sadler's Wells Theatre and later to the Savoy Theatre. Richardson played the hero, Tom Wrench, a small-part player who wants to write about "real people". He had a song, "Walking On", lamenting his lack of scope in the company, in which he explains that as a "walking gentleman" he will be forever "walking on", whilst Rose Trelawney will go on to be a star.

On leaving the RSC, he played Professor Henry Higgins in the 20th anniversary Broadway revival of My Fair Lady (1976) and received the Drama Desk Award for Outstanding Actor in a Musical and a nomination for the Tony Award for Best Actor in a Musical. He also appeared on Broadway as onstage narrator in the original production of Edward Albee's play Lolita (1981), an adaptation of Vladimir Nabokov's book that was not critically well received.

His first major role was his appearance as Bill Haydon ("Tailor") in the BBC adaptation of Tinker Tailor Soldier Spy (1979). He played the part of Bernard Montgomery in Churchill and the Generals in 1979, a BBC television videotaped play concerning the relationship between Winston Churchill and generals of the Allied forces between 1940 and 1945.

In the 1980s, he became well known as Major Neuheim in the award-winning Private Schulz and as Sir Godber Evans in Channel 4's adaptation of Porterhouse Blue. Richardson also performed the role of Sherlock Holmes for two of six planned BBC television movies, The Sign of Four and The Hound of the Baskervilles, in 1983, which were both critically acclaimed. He appeared in Brazil (1985) and played Jawaharlal Nehru in the television serial, Lord Mountbatten: The Last Viceroy (1986). He portrayed Anthony Blunt, the Soviet spy and Surveyor of The King's Pictures in the BBC film Blunt: the Fourth Man (1986) opposite Anthony Hopkins as Guy Burgess. In 1988, he played Edward Spencer, the eccentric and oblivious English landowner in 1920s' Ireland in Troubles, from J. G. Farrell's award-winning novel. In 1987, he played a variation on this role, when he portrayed the Bishop of Motopo in the non-musical television film Monsignor Quixote, based on Graham Greene's modernized take on Don Quixote. He played Sir Nigel Irvine in John Mackenzie's adaptation of Frederick Forsyth's novel The Fourth Protocol (1987).

He was appointed Commander of the Order of the British Empire (CBE) in the 1989 New Year Honours.

Other roles in this period include Polonius in Rosencrantz & Guildenstern Are Dead (1990), wine dealer Sir Mason Harwood in The Year Of The Comet (1992), the French ambassador in M. Butterfly (1993), Martin Landau's butler in B*A*P*S (1997), a malevolent alien in Dark City (1998), The Kralahome in The King and I (1999), Cruella de Vil's Barrister, Mr. Torte QC, in the live-action film 102 Dalmatians (2000), and a corrupt aristocrat in From Hell (2001).

In 1999, Richardson became known to a young audience as the main character Stephen Tyler in both series of the family drama The Magician's House (1999–2000). Following this he played Lord Groan in the major BBC production Gormenghast (2000), and later that year he starred in the BBC production Murder Rooms: The Dark Beginnings of Sherlock Holmes (2000–2001) (screened in PBS's Mystery! series in the US), playing Arthur Conan Doyle's mentor, Dr. Joseph Bell, a role he welcomed as an opportunity to play a character from his native Edinburgh. He had earlier played Sherlock Holmes in television versions of The Hound of the Baskervilles (1983) and The Sign of Four (1983). He once more returned to fantasy in the recurring role of the villainous Canon Black in the short-lived BBC cult series Strange (2003).

In 2002, Richardson joined Sir Derek Jacobi, Sir Donald Sinden and Dame Diana Rigg in an international tour of The Hollow Crown. A Canadian tour substituted Alan Howard for Jacobi and Vanessa Redgrave for Rigg. He also appeared in The Creeper by Pauline Macaulay at the Playhouse Theatre in London, and on tour. His last stage appearance was in 2006 as Sir Epicure Mammon in The Alchemist at the National Theatre in London.

In 2005, he took on the role of a curiously detached Chancellor in the television drama Bleak House. He also played the Judge in the family-based film, The Adventures of Greyfriars Bobby (2005). Additionally in that year, he appeared in ITV's main Christmas drama The Booze Cruise 2, playing Marcus Foster, a slimy upper class businessman forced to spend time with "the lower classes". He returned to this role for a sequel the following Easter.

Dame Helen Mirren dedicated her 2006 Best Actress BAFTA award for her portrayal of Queen Elizabeth II in the film The Queen to Ian Richardson. In her acceptance speech she said that, without his support early in her career, she might not have been so successful, before breaking down and leaving the stage. Other tributes and reminiscences by Richardson's colleagues are offered in a memoir by Sharon Mail, We Could Possibly Comment: Ian Richardson Remembered (2009).

Richardson died in his sleep of a heart attack on the morning of 9 February 2007, aged 72. According to his agent, he had not been ill and had been due to start filming an episode of Midsomer Murders the following week, playing Victor Godbold, Lord Holme in the episode "Death in a Chocolate Box"; Edward Petherbridge took over the role. Richardson was survived by his wife, Maroussia Frank, an Actress, and two sons. One son, Miles, is an actor with the Royal Shakespeare Company. Richardson's widow and his son Miles placed his ashes in the foundations of the auditorium of the Royal Shakespeare Theatre in Stratford, during its renovations in 2008.

He played one musical role on film – the Priest in Man of La Mancha, the 1972 screen version of the Broadway musical. Also in 1972, he played Anthony Beavis in the television series Eyeless in Gaza. In 1974, he played King Richard II/Bolingbroke in Richard II part of the Camera Three television series. In 1978, he played Robespierre in the BBC's Play of the Month production of Danton's Death. In 1979, he played Field Marshal Sir Bernard Montgomery in the TV miniseries Ike