A native of Miami, Florida, Howser attended college at Florida State University, where he twice received honors as an All-America shortstop and set a school record with a batting average of .422 in 1956. Drafted by the Kansas City Athletics, he hit .280, stole 37 bases, scored 108 runs, and led American League shortstops in putouts and errors in his rookie season. For this, he was selected to the 1961 All-Star team and named The Sporting News rookie of the year.

His production declined in the following two years, and his only other season as a regular was with the Cleveland Indians in 1964. His major league career spanned eight seasons with three clubs: Kansas City, Cleveland, and the New York Yankees.

Howser was more successful as a manager, never finishing lower than second place during his seven-year managerial career. He made his debut in 1978, managing one game with the Yankees. In 1980 he became a full-time manager of the team, taking them to the AL Eastern Division championship with a 103-59 record but losing to the Kansas City Royals in the playoffs. Yankees owner George Steinbrenner fired him following the postseason.

Meanwhile, Kansas City, his postseason rival, hired him to manage the last 33 games of the strike-shortened 1981 season. Under Howser, the Royals finished second in 1982 and 1983. Prior to the 1984 season, their clubhouse ravaged by drug problems, started disassembling their team and starting over. Kansas City expected 1984 to be a rebuilding year, but Howser guided the young team to a division title. The Royals were defeated by the Detroit Tigers in the American League Championship Series, three games to none.

The following year, Howser guided the Royals to their first and to date, only World Series title, defeating the St. Louis Cardinals in seven game series which featured a controversial call by umpire Don Denkinger in Game 6. Howser guided the AL to a 3-2 victory, starting a 20-year stretch that has seen the junior circuit go 15-4-1 in the Mid-Summer Classic after going 2-21 from 1963 through 1985.

As manager of the defending AL champions, Howser managed the 1986 All-Star game at the Astrodome in Houston. Broadcasters noticed he was messing up signals when he changed pitchers, and Howser later admitted he felt sick before the game. It was the last game he would manage in the major leagues, as he was diagnosed with a brain tumor and underwent surgery.

Howser attempted a comeback during spring training of 1987, but quickly found he was physically too weak and abandoned the attempt in late February, when Billy Gardner took over. Three months later, he died in St. Luke's Hospital in Kansas City, Missouri at the age of only 51, and was buried in Tallahassee, Florida.

On July 3, 1987, Howser's number 10 became the first number retired by the Kansas City Royals. Also in that year, the St. Petersburg Area Chamber of Commerce established the Dick Howser Trophy, college baseball's equivalent of college football's Heisman Trophy, in Howser's honor.

Florida State University's baseball team plays on Mike Martin Field at Dick Howser Stadium, named in his honor, and he is honored with a bronze bust on the stadium grounds.