After joining the New York Giants, he hit .300 three more times and became the first NL shortstop to hit 20 home runs more than once. His .411 career slugging average was the seventh highest by an NL shortstop at his retirement, and his 126 home runs placed him behind only Ernie Banks and Travis Jackson. After leading the NL in putouts and double plays three times each, he ended his career with the seventh most double plays (933) and tenth highest fielding percentage (.960) in league history. He went on to become the third manager to win pennants with both National and American League teams.
He was named the MLB 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, though 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 a boon for the Giants. 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 since 1937; he hit .417 in the World Series against the New York Yankees, including a three-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.
Dark had a role in one of baseball history's weirdest plays. It took place during a game played on June 30, 1959, between the St. Louis Cardinals and Chicago Cubs. Stan Musial was at the plate, with a count of 3-1. Bob Anderson's next pitch was errant, evading catcher Sammy Taylor and rolling all the way to the backstop. Umpire Vic Delmore called ball four, but Anderson and Taylor contended that Musial foul tipped the ball. Because the ball was still in play, and because Delmore was embroiled in an argument with the catcher and pitcher, Musial took it upon himself to try for second base. Seeing that Musial was trying for second, Dark ran to the backstop to retrieve the ball. The ball wound up in the hands of field announcer Pat Pieper, but Dark ended up getting it back anyway. Absentmindedly, however, Delmore pulled out a new ball and gave it to Taylor. Anderson finally noticed that Musial was trying for second, took the new ball, and threw it to second baseman Tony Taylor. Anderson's throw flew over Tony Taylor's head into the outfield. Dark, at the same time that Anderson threw the new ball, threw the original ball to shortstop Ernie Banks. Musial, though, did not see Dark's throw and only noticed Anderson's ball fly over the second baseman's head, so he tried to go to third base. On his way there, he was tagged by Banks, and after a delay he was ruled out.
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 1,828 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.
In a 1969 poll, Giants fans selected Dark as the greatest shortstop in team history.
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 weathered the imbroglio, but Giants owner Horace Stoneham fired him during the sixth inning of the last game of the season, with the team about to finish in fourth place. 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, Jr. for his behavior on a team flight. (Finley also released first baseman Ken Harrelson, who had been quoted as saying that Finley was a menace to the sport.)
Dark was hired to manage the Cleveland Indians in 1968 by Vernon Stouffer; after an initial third-place season, he was given the additional duties of general manager, but having the field manager negotiate the players' contracts proved an untenable situation. The Indians returned to their losing ways and Dark was fired 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 1980, Dark penned an autobiography (with John Underwood) entitled When in Doubt, Fire the Manager, published by E. P. Dutton, the back cover of which included endorsements by Ted Williams and Gene Mauch. In it, Dark focused mostly on his career as manager, especially of the Oakland A's under Charlie Finley, and how his conversion to Christianity affected how he chose to manage his teams.
Dark was married twice. His first marriage to Adrienne Managan, ended in divorce. His second marriage to Jocelyn Troy Dark of Easley, South Carolina lasted 44 years until his death at the age of 92. Dark had four children from his first marriage and two adopted children from his second marriage. At his death he was survived by his wife Jocelyn, his children, 20 grandchildren, and three great grandchildren.