By the age of ten Hawkins had joined the local operatic society, and made his stage debut in Patience by Gilbert and Sullivan. His parents enrolled him in the Italia Conti Academy and whilst he was studying there he made his London stage debut, when aged eleven, playing the Elf King in Where the Rainbow Ends at the Holborn Empire on Boxing Day, December 1923, a production that also included the young Noël Coward. The following year aged 14 he played the page in a production of Saint Joan by George Bernard Shaw. Five years later he was in a production of Beau Geste alongside Laurence Olivier.

Films in the late 1930s included Beauty and the Barge (1937), The Frog (1937) (which Hawkins played on stage), Who Goes Next? (1938), A Royal Divorce (1938), Murder Will Out (1939) and The Flying Squad (1940).

Hawkins married Actress Jessica Tandy in 1932, and the couple divorced in 1940. Together they had one daughter, Susan Hawkins (b. 1934). In 1947, Hawkins married Doreen Lawrence (1919–2013), and they remained married until his death in 1973. Together they had three children, Caroline (b. 1955), Andrew, and Nicholas Hawkins.

Stage roles included Iron Mistress (1934) by Arthur Macrae; then an open air Shakespeare festival – As You Like It (1934) (with Anna Neagle), Twelfth Night (1934), Comedy of Errors (1934). Some of these productions were done on radio. The Maitlands by Ronald Mackenzie (1934) was for John Gielgud's company. He was Horatio to Gielgud's Hamlet (1934). He also appeared in Accidentally Yours by Clifford Grey (1935), The World Waits by Clifford Hummel (1935), Coincidence by Bryce Robertson (1935) and The Frog (1935).

Theatre appearances included A Winter's Tale (1937), Autumn by Margaret Kennedy and Gregory Ratoff (1937, with Flora Robson for Basil Dean), The King's Breakfast by Rita Welman and Maurice Marks (1937–38), No More Music by Rosamund Lehman (1938), Can We Tell? by Robert Gore Brown (1938), Traitors Gate by Norma Stuart (1938) and Dear Octopus by Dodie Smith (1938–39).

During the Second World War Hawkins served as an officer with the Royal Welch Fusiliers. He became a colonel in ENSA for India and Southeast Asia. During his military Service he made The Next of Kin (1942) for Ealing Studios.

Hawkins left the army in July 1946. Two weeks later he appeared on stage in The Apple Cart at ten pounds a week. The following year he starred in Othello, to a mixed reception.

The association began badly when Hawkins was cast in Korda's notorious flop Bonnie Prince Charlie (1948) as Lord George Murray. However he followed it with a good role in the successful, highly acclaimed The Fallen Idol (1948) for Carol Reed. Also acclaimed was The Small Back Room (1949), for Powell and Pressburger; he impressed as the villain in State Secret (1950), for Sidney Gilliat with Douglas Fairbanks Jnr.

During the 1950s, British exhibitors consistently voted Hawkins one of the most popular local stars in the country in the annual poll conducted by the Motion Picture Herald:

Hawkins became a star with the release of three successful films in which he played stern but sympathetic authority figures: Angels One Five (1951), as an RAF officer during the war; The Planter's Wife (1952), as a rubber planter combating communists in the Malayan Emergency (with Claudette Colbert); and Mandy (1952), the headmaster of a school for the deaf. All films ranked among the top ten most popular films at the British box office in 1952 and British exhibitors voted him the fourth most popular British star at the local box office.

He had a guest role in Twice Upon a Time (1953) for Emeric Pressburger. He followed this with two mildly popular dramas – The Intruder (1953) and Front Page Story (1954).

"I'm tired of playing decent fellows", he said in a 1954 interview, "with stiff upper lip and even stiffer morals. I'm going to kill them off before they kill me as an actor. And I want stories written for me, not rejects intended for other fellows... I just inherit them from other people. Often, I find they've left the name of the actor originally suggested for the role. Always the same old names . . . Errol Flynn, Gregory Peck . . . five or six others. Before the script reaches them, somebody remembers me — especially if it's one of those infernally nice characters."

He returned home to make an Ealing comedy, Touch and Go (1955), which was not particularly popular. He was more comfortably cast as a police officer in The Long Arm (1956) and a test pilot in The Man in the Sky (1957). He was an insurance investigator in Sidney Gilliat's Fortune Is a Woman (1957).

Hawkins's career received a major boost when given the third lead in The Bridge on the River Kwai (1957), supporting william Holden and Alec Guinness. This was a massive hit and highly acclaimed.

Hawkins played the lead role a film for John Ford, Gideon's Day (USA title: Gideon of Scotland Yard) (1958), playing a police officer. He had a good role as a double agent in a war film, The Two-Headed Spy (1958) then was given another third lead in a Hollywood blockbuster Ben-Hur (1959), playing the Roman admiral who befriends Charlton Heston. It was even more successful than Bridge on the River Kwai.

He appeared as one of The Four Just Men (1959) in the Sapphire Films TV series for ITV, one of the most ambitious British TV series ever made. He also played the lead in a version of "The Fallen Idol" for American TV.

"There are not all that number of mature leading men around", he said in a 1961 interview. "There seems to be a generation missing. I think people quit going into the acting profession. A lot of them drifted out during the war. And then when the war was over it was difficult for them to get back into the theatre."

He was in another big hit in Lawrence of Arabia (1962), as General Allenby. Rampage (1963) was less distinguished but Zulu (1964) gave him a good role as a cowardly priest; it was however clearly a support part and Hawkins' days as a star seemed to be over.

He had support parts in The Third Secret (1964), Guns at Batasi (1964) and Lord Jim (1965). Masquerade (1965) gave him a lead opposite Cliff Robertson. He made some appearances on US TV: "To Bury Caesar" with Pamela Brown in 1963 and "Back to Back" for The Bob Hope Theatre. He also appeared in Judith (1966), and The Poppy Is Also a Flower (1966).

In December 1965, Hawkins was diagnosed with throat cancer. His entire larynx was removed in January 1966. In March of that year he appeared at a royal screening of Born Free attended by the Queen and received a standing ovation.

In 1967 it was reported that he would direct Peter O'Toole in St Patrick's Battalion in Mexico but the film was not made.

Instead he resumed his acting career, with his voice dubbed and dialogue kept to a minimum: Shalako (1968) and Great Catherine (1968). In Oh! What a Lovely War (1969), playing Emperor Franz Joseph I of Austria, he had no lines at all. He had an operation to restore his voice in 1968. It did not work; Hawkins could talk but only in a croaking voice.

Some rare comedies followed: Monte Carlo or Bust (1969), Twinky (1970), The Adventures of Gerard (1970). There was more typical fare: Waterloo (1970), Jane Eyre (1970), The Beloved (1971), When Eight Bells Toll (1971), Nicholas and Alexandra (1971) and Kidnapped (1971).

Hawkins also produced the film adaptation of Peter Barnes's The Ruling Class (1972), with Peter O'Toole and Alastair Sim.

In May 1973 Hawkins undertook an experimental operation on his throat to insert an artificial voicebox. He started haemorrhaging and was admitted to St Stephen's Hospital, Fulham Road, London in June, forcing him to drop out of The Tamarind Seed (1974), in which Hawkins was to have played a Russian general. He died on 18 July 1973, of a secondary haemorrhage. He was 62.