Born in Kennett, Missouri, he was a versatile player during his pro career (1935–1942; 1944–1954) who spent two seasons in Major League Baseball as a utility infielder for the 1946–1947 Philadelphia Athletics.

Handley batted and threw right-handed; he stood 5 feet 10 inches (1.78 m) tall and weighed 165 pounds (75 kg).

Gene Handley spent ten seasons in minor league baseball before winning a job with the 1946 Athletics.

He broke into the professional game as an outfielder, but he soon converted to a third baseman, and also played second base and shortstop in the minors.

After his playing career, Handley was a minor league manager, then a longtime scout, for the Chicago Cubs, working in the Chicago organization for 54 years and signing players such as 1962 NL Rookie of the Year Ken Hubbs, Dick Ellsworth, Mike Krukow and Pete LaCock.