Cuthbert began running at age eight and was trained by a schoolteacher in the little New South Wales town in which she grew up. As a teenager, she performed well but laboured in the shadow of her teammate Marlene Matthews, whose times were superior to hers. Cuthbert was so uncertain about her performance that she bought tickets to attend the Melbourne Games as a spectator. She need not have worried: in the first round of the 100-metre event she smashed the world record with a time of 11.4 sec, leading the field by 1.5 metres (5 feet). Although she was instantly hailed as a national hero, the unassuming 18-year-old Cuthbert quietly prepared for her next race, the 200 metres, which she won four days later with a time of 23.4 sec. Several days after that, she anchored the Australian 4 × 100-metre relay team, earning her third gold medal of the 1956 Games.

During the years 1956–63, Cuthbert held 12 world records in races at distances of 60 to 400 metres. A pulled hamstring forced her to miss the 1960 Olympics in Rome, but in 1964 she won the first women's Olympic 400-metre race with a time of 52 sec. She later described her performance as “the only perfect race I have ever run.” In 1966 her autobiography, Golden Girl, was published.