Dark attended LSU, and was a football standout there as well as a great baseball player, being drafted by the Philadelphia Eagles. He was named the Rookie of the Year and finished third in the MVP voting in 1948 after playing a vital part of the Braves' unlikely run to the pennant, their first since 1914; but he hit only .167 in the World Series loss to the Cleveland Indians. He was traded after the 1949 season, which turned out to be one of the best trades in Giants history and one of the worst in Braves history. Dark was immediately named team captain by manager Leo Durocher, and had several great seasons in New York. In 1951 he batted .303 with 114 runs and a league-leading 41 doubles as the Giants won their first pennant in 14 years; he hit .417 in the World Series against the New York Yankees, including a 3-run home run in Game 1, though the Giants lost in six games. He followed up with seasons hitting .301 and .300 in 1952-53, scoring 126 runs with 23 home runs and 41 doubles in the latter season. In 1954 he batted .293 with 20 home runs and was fifth in the MVP voting as the Giants won another pennant; in the World Series against the heavily favored Indians, he batted .412 with a hit in every game, and the Giants pulled off an astonishing sweep to win their first championship since 1933. He was the NL's starting shortstop for the All-Star game in 1951, 1952, and 1954. In 1955 he was awarded the first Lou Gehrig Memorial Award, given to the player who best exemplified Gehrig's character and integrity both on and off the field.

In June 1956 he was traded to the St. Louis Cardinals in a nine-player deal; he continued to hit well, and led the NL in putouts and double plays for the third time in 1957. He was traded to the Chicago Cubs in May 1958, batting .295 over the remainder of the season and .264 in 1959; with Ernie Banks at shortstop, the Cubs shifted Dark to third base, where he remained in his last seasons. In January 1960 he was traded with two other players to the Philadelphia Phillies in exchange for Richie Ashburn; after hitting .242 in 55 games, he was traded back to the Braves (now in Milwaukee) in June, and hit .298 in his final 50 games. On October 31 of that year, he was traded back to the Giants (who had moved to San Francisco two years earlier), who wanted him as their new manager rather than as a player. Dark retired with a .289 career batting average, 2089 hits, 1064 runs and 757 runs batted in over 1828 games played. According to baseball writer Bill James, he may have lost a Hall of Fame career due to his debut being delayed by his military service during World War II.

Dark quickly became a successful manager, winning a pennant with the Giants in 1962, but losing the 1962 World Series in seven games to the Yankees. In 1964 he became embroiled in controversy when he was quoted in Newsday as complaining about the number of black and Hispanic players on the team and saying, "They are just not able to perform up to the white player when it comes to mental alertness." He responded that he had been severely misquoted; Willie Mays, whom he had named as team captain, came to his defense and calmed the team, and Jackie Robinson further noted, "I have found Dark to be a gentleman and, above all, unbiased. Our relationship has not only been on the ballfield but off it." Dark survived the controversy, but was fired after the season when Giants owner Horace Stoneham learned of an extramarital affair. He was hired as an assistant to Kansas City Athletics owner Charlie Finley in 1965, and became that team's manager the next season, but was dismissed in August 1967 in a disagreement over player discipline after Finley fined and suspended pitcher Lew Krausse for his behavior on a team flight. (Finley also released first baseman Ken Harrelson, whom he descibed as a menace to the sport.)

Dark was hired to manage the Cleveland Indians in 1968; after an initial third-place season, he departed in mid-1971 with the team in last place. In the meantime, the Athletics had moved to Oakland, and after manager Dick Williams resigned following consecutive World Series triumphs in 1972-73, Finley rehired Dark. He guided the A's to a third straight championship in 1974, joining managers Joe McCarthy and Yogi Berra by winning pennants in both leagues, but was again fired after losing the 1975 American League Championship Series. He was hired by the San Diego Padres in mid-1977, but left the team after that season following a fifth-place finish. He ended his career with a 994-954 record, despite the decided weakness of his teams in Cleveland and San Diego. In a 1969 poll, Giants fan selected him as the greatest shortstop in team history.