A native of Huntsville, Ontario, Selkirk batted left-handed and threw right-handed, standing 6 feet 1 inch (1.85 m) tall and weighing 182 pounds (83 kg) (13 stone).
He earned the nickname "Twinkletoes" for his distinctive way of running on the balls of his feet.
During his nine years of Major League Baseball service, all with the Yankees, he appeared in 846 games and hit .290 (.265 in 21 World Series games), with 108 regular-season home runs and 810 hits.
After military service in World War II (in the United States Navy, despite his Canadian citizenship), Selkirk managed at the Class A and Triple-A levels for the Yankees, and at Triple-A in the farm system of the Milwaukee Braves.
The Senators were chronically short of funds and never developed a strong farm system, forcing Selkirk to acquire players (such as the great slugger Frank Howard) through trades and fill out the roster with waiver-price acquisitions. Nonetheless, Washington improved every year from 1963 through 1967, but when the team's field manager, Gil Hodges, departed for the New York Mets after the '67 campaign, the Senators regressed and fell back into the American League basement. The death of one of the club's owners forced the sale of the team in the autumn of 1968, and Selkirk was fired during the transition. He then returned to the Yankees as a scout.
He was, arguably, the greatest Canadian-born baseball player of the first half of the 20th century.
Selkirk is mentioned in August Wilson's 1987 Pulitzer Prize-winning play, "Fences." The protagonist, Troy, confident that he can do better than white ballplayers in the majors, alludes to Selkirk and his .269 average.