Born in Mexborough, Yorkshire, Hawthorn was educated at Ardingly College and later studied at Chelsea technical college before an apprenticeship with a commercial vehicle manufacturer. His father Leslie owned the Tourist Trophy Garage in Farnham, franchised to supply Jaguar and Ferrari, and had raced motorcycles; his son inherited the business after Leslie died in a road accident in 1954. Hawthorn made his competition debut in 1950 at the Brighton Speed Trials and progressed through national events at Goodwood and Dundrod before switching to single-seaters in 1952.
Hawthorn's performances in a Formula Two Cooper-Bristol at Goodwood in 1952 brought him to Enzo Ferrari's attention, and Ferrari offered him a works drive. He made his Formula One debut at the 1952 Belgian Grand Prix at Spa, finishing fourth. In 1953 at Scuderia Ferrari he produced his defining early performance at the French Grand Prix at Reims, outmanoeuvring Juan Manuel Fangio in what was described as the race of the century — the top four finishers covered by five seconds after 60 laps. He finished fourth in the championship that year.
After a year at Vanwall following his father's death (requiring more time at the family garage), then a return to Ferrari, Hawthorn joined Jaguar for 1955 and won the 24 Hours of Le Mans. That race, however, was catastrophically overshadowed: Hawthorn's braking manoeuvre in front of Lance Macklin's car triggered a chain of events that led Pierre Levegh's Mercedes to crash into spectators, killing 83 people. An official inquiry found Hawthorn was not responsible, ruling it a racing incident. The disaster prompted motorsport bans in France, Switzerland, Germany, and other countries pending safety improvements.
Hawthorn returned to Ferrari for 1957 and formed a close friendship with teammate Peter Collins. In 1958, driving the Ferrari Dino 246, he won the championship despite securing only one race victory — the French Grand Prix at Reims — against four wins by Stirling Moss in a Vanwall. Hawthorn accumulated his margin primarily through consistency and, critically, through a gesture of sportsmanship from Moss.
At the 1958 Portuguese Grand Prix, Hawthorn was disqualified for bump-starting his stalled car in the wrong direction. Moss, who had won the race, interceded with officials on Hawthorn's behalf, and the disqualification was reversed. Hawthorn added an extra point for fastest lap in the same race. Those points, combined with Moss's second-place total at season's end, gave Hawthorn the championship by a single point — a margin that made Moss's act of honesty the difference between winning and losing.
The 1958 season was also marked by the deaths of Ferrari teammates Luigi Musso (fatally injured at the French Grand Prix) and Peter Collins (killed at the German Grand Prix). The losses profoundly affected Hawthorn, and after winning the championship at the Moroccan Grand Prix he immediately announced his retirement.
Hawthorn shares with Keke Rosberg the Formula One record for the fewest Grand Prix victories in a title-winning season, having secured the championship with just one win. He was noted during his career for wearing a bow tie while racing, earning him the nickname "Le Papillon" (The Butterfly) from the French press.
On 22 January 1959, three months after his retirement, Hawthorn died when his Jaguar 3.4-litre saloon left the road on the A3 Guildford bypass in wet conditions. An inquest returned a verdict of accidental death. His acquaintance Rob Walker, the motor racing team manager who was also driving on the same road at the time, admitted in a 1988 interview that the two had been racing each other, though he had not disclosed this at the coroner's inquest. Evidence also suggested Hawthorn had suffered blackouts related to a kidney condition, having lost one kidney to infection by 1955.
The Hawthorn Memorial Trophy has been awarded annually since 1959 to the most successful British or Commonwealth driver in Formula One, with Lewis Hamilton its most frequent recipient. There is a corner named after Hawthorn at Brands Hatch and another at Croft racing circuit. A statue at Goodwood commemorates him as the UK's first Formula One World Champion. The Tourist Trophy Garage in Farnham where he lived and worked still bears his name.