He was selected in the second round (22nd overall) of the 1953 NFL draft by the New York Giants, but declined due to a nerve problem in his throwing arm and served in the U.S. Army Corps of Engineers as quarterback of the Fort Hood team for 1953.

Although selected by the Giants, Crowder went to Canada in 1953 and played the first half of the season with the Edmonton Eskimos, alternating starts at quarterback with Claude Arnold.

He was cut by head coach Darrell Royal because of limitations on the number of American players that a team could carry past a certain date.

Crowder was an assistant coach under Red Blaik at Army in 1955 and for Bud Wilkinson back at Oklahoma for seven seasons (1956–1962).

With a final annual salary of $52,800, Crowder stepped down as athletic director in 1984, succeeded by Bill Marolt.