Before taking up the study of law in 1940, White achieved a national reputation as a quarterback and halfback on the University of Colorado football team, earning the nickname “Whizzer.” In 1937 he was the runner-up for the Heisman Trophy, the award for the best collegiate football player. After graduating from Colorado in 1938, White became the highest-paid player in the National Football League (NFL), signing a one-year contract with the Pittsburgh Pirates (now the Steelers), and during the 1938 season he led the NFL in rushing. In 1939 White attended the University of Oxford as a Rhodes scholar but returned to the United States after the start of World War II. He then played two seasons with the Detroit Lions (1940–41) while attending Yale Law School, from which he graduated with high honours in 1946.

White served for a year as law clerk to Chief Justice Fred M. Vinson (Vinson, Fred M.) before joining a law firm in Denver. In 1960 he was active in the presidential campaign of John F. Kennedy (Kennedy, John F.), an old friend, and in 1961 was made assistant attorney general under the president's brother Robert Kennedy (Kennedy, Robert F.). In 1962 President Kennedy appointed him to the U.S. Supreme Court. Despite his liberal political background, White's role on the court was generally described as moderate or relatively conservative. He dissented from many of the court's liberal rulings, including Wade (Roe v. Wade) (1973), which legalized abortion nationwide, and Arizona (Miranda v. Arizona) (1966), which established a code of conduct for police during interrogations.