Dudley was drafted in the 1942 NFL Draft with the first overall pick by the Pittsburgh Steelers. During the 1942 season, he led the league in rushing with 696 yards on 162 carries and was then named to the All-Pro team. He also completed 35 of 94 passes for 438 yards and two touchdowns, punted 18 times for a 32.0 average, returned 20 punts for 271 yards (14.0 avg), and ran back 11 kickoffs for 298 yards (27.0 avg), scoring once. In the first game of his professional career, Dudley ran for a 55-yard touchdown and in his second game scored on a kickoff return.
In 1942, the U. S. armed services began drafting all eligible young men to fight in World War II. Dudley originally enlisted and was sworn into the Naval Air Corps; however, they found out he needed to have his parents' consent, since he was not yet 21. Dudley then enlisted in U. S. Army Air Corps in September 1942, but there was an influx of recruits and Dudley was told he would have to wait three months before he began training. This delay made it possible for him to finish his rookie season with the Steelers.
Dudley went through basic training in Florida and then attended flight school in Texas. He then joined the Army's football team. In 1944, Dudley helped his team to a 12–0 record and was named the Most Valuable Player. At the end of the war, Dudley was shipped to the Pacific and flew two supply missions. He was then sent to Hawaii where the Army selected him to play in three more football games against All-Star teams.
Dudley returned to Pittsburgh that fall and rejoined the Steelers's team for the last four games of the 1945 season. In a game against the Chicago Cardinals, he ran for two touchdowns and kicked for two additional points and became the Steelers' leading scorer for that season. He also rushed for 204 yards and returned three kickoffs for 65 yards.
In 1946, the Steelers hired a new coach Jock Sutherland and Dudley scored 48 points, which contributed to the Steelers' 5–5–1 record. During that season, he became the league leader in rushing (604 yards), interceptions (10 total which he returned for 242 yards) and punt returns (27 total for 385 yards). In doing this, Dudley became the only NFL player to lead in four unique statistical categories. He was named All-Pro and was awarded the NFL's Most Valuable Player Award. Dudley became the first (and as of 2007, only) person to win MVP awards in college, service, and professional levels.
Dudley was traded to the Detroit Lions after 1946, where he was offered a three-year contract and $20,000 a season. He was elected captain of his team all three years, 1947–1949. During his first year with the Lions, the team finished last. On October 19, 1947, against the Chicago Bears, Dudley returned a punt for an 84-yard touchdown. During 1947, he scored 13 touchdowns; seven on pass receptions, four on runs from scrimmage, one on a punt return, one on kickoff return and throwing two. In his last season with the Lions, he led Detroit in scoring for the third year in a row.
At the end of the 1949 season, Lions coach Bo McMillin traded Dudley to the Washington Redskins, where he played for three seasons, during which he led the team in scoring every year. On December 3, 1950, Dudley fielded a 60-yard punt kicked by Steelers' player Joe Geri. He ran over 30 yards before he reached his hands out of bounds, while keeping both feet in bounds, and caught the punt at the Redskin's four-yard line, and then ran it for a 96-yard touchdown. Dudley took a break during the 1952 season but returned in 1953. He retired at the end of the season due to knee injuries and an overall physical deterioration.
Dudley was named first- or second-team All-NFL six times in his career and was named to three Pro Bowls. During his nine pro seasons, Dudley gained 3,057 yards on 765 rushing attempts, a 4.0 average, and scored 20 touchdowns; caught 123 passes for 1,383 yards and 18 touchdowns; returned 124 punts for 1,515 yards and three touchdowns; ran back 78 kickoffs for 1,743 yards and one touchdown; intercepted 23 passes and returned them for 459 yards and two touchdowns; and punted 191 times for a 38.2-yard average. He added 121 extra points and 33 field goals to his 44 touchdowns for a total of 484 points. Dudley led his team in scoring during every one of his nine NFL seasons.
Dudley is the only player ever with a rushing touchdown, touchdown reception, punt return for touchdown, kickoff return for touchdown, interception return for touchdown, fumble return for a touchdown, and a touchdown pass. He also had a touchdown via lateral and kicked PATs and field goals.
After retiring, Dudley was a scout for the Steelers and the Lions. In 1951, he then entered the insurance business in Lynchburg, Virginia with his brother Jim.
Dudley was elected to the College Football Hall of Fame in 1956, the Pro Football Hall of Fame in 1966, and the Virginia Sports Hall of Fame in 1972. The Downtown Club of Richmond, Virginia has sponsored the Bill Dudley Award since 1990, awarded each year to the state's top college football player.
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