By the time Davis made the majors, the Dodgers had moved to Los Angeles; he debuted with a pinch-hitting appearance on September 22, 1959. He batted .276 in his 1960 rookie season, and .278 in 1961, before enjoying his breakout year in 1962. His .346 batting average edged out Frank Robinson's .342 for the National League batting crown; he also had career bests with 27 home runs, 120 runs and 9 triples as the Dodgers finished the regular schedule tied for first place with the San Francisco Giants, but lost a three-game playoff. He finished third in the MVP balloting, with teammate Maury Wills winning the award and Willie Mays finishing second. In 1963 he won his second batting title, edging Roberto Clemente by 6 points, and finished eighth in the MVP balloting. In the 1963 World Series, the Dodgers swept the New York Yankees; batting cleanup, Davis hit .400 in the Series, tripling twice in Game 2 and driving in the only run of the 1-0 Game 3 victory, his first-inning single off Jim Bouton driving in Jim Gilliam.
To date, Davis' back-to-back batting titles are the only two in the Dodgers' Los Angeles history. Only two right-handed hitters have won multiple National League batting titles since: Bill Madlock with four, and Roberto Clemente with four. Davis won the batting titles while playing his home games at Dodger Stadium—a reputed "pitcher's park."
Davis slumped to .275 in 1964 as the Dodgers finished out of contention for the pennant. On May 1, 1965, against the visiting Giants, he broke and dislocated his ankle sliding into second base while trying to break up a double play and was lost for the remainder of the season. Three days later the Dodgers called up Lou Johnson to replace him. They won the World Series that year, defeating the Minnesota Twins in seven games. Davis rebounded in 1966, batting .313 (but with only three home runs and 27 RBIs in 313 at bats). Los Angeles was swept by the Baltimore Orioles in the World Series, with Davis starting only two of the four games and batting .250.
In October 1968 Davis was selected by the Seattle Pilots in the expansion draft. During the 1969 season he batted .271 in 123 games with the Pilots before being traded to the Houston Astros, where he hit .241; his 20 stolen bases that year were a career high. He began 1970 with Houston, hitting .282, before his contract was sold to the Oakland Athletics in June; he hit .290 with the A's before being sent to the Chicago Cubs for the last two weeks of the season. The Cubs released him in December, and he re-signed with the A's as a free agent, rebounding with a .324 campaign in 1971. But Oakland released him at the end of 1972 spring training; he signed with the Cubs again in July, but played only a month before being traded to the Baltimore Orioles, where he would spend the next three seasons. In Baltimore, he served as the designated hitter from 1973–75, finishing third in the 1973 batting race with a .306 mark and placing tenth in the MVP vote; in 1974 he was second in the American League with 181 hits. In 1974 he won the Outstanding Designated Hitter Award (later renamed for Edgar Martínez). He played in two American League Championship Series (both times, in 1973 and 1974, the Orioles lost to the eventual World Series champion Athletics). The Orioles released him in 1976 spring training, and he signed with the Yankees but did not play for them. From June to September he hit .265 with the California Angels before ending the season with the Kansas City Royals. He retired after being released by the Royals on January 17, 1977, having played for ten different teams in eighteen seasons. He occasionally expressed resentment for his numerous moves, remarking late in his career: "I'm very bitter, bitter as hell. Why do I keep getting released? Don't ask me no reason why." But he conceded his reputation as having a casual style of play, noting, "the lazier I felt the better I hit," and admitting that he often went into the clubhouse to read and even to shave between at bats as a DH with Baltimore. After his retirement from baseball as a player, he served as a Seattle Marinerscoach in 1981 and published a book called Tales From the Dodgers Dugout  in 2005.
"For two years (1962 and 1963), Tommy was the best hitter in baseball. He just didn't get the recognition. He was part of a team that had a lot of good parts to it."'