Crowder was an assistant coach under Red Blaik at Army in 1955 and for Bud Wilkinson back at Oklahoma for seven seasons (1956–1962). In January 1963 at age 31, he became the head coach of the Buffaloes; his initial contract was for five years at $15,000 per year.[3][4] He restored the program's respectability and earned national respect while rebuilding the program.
In Crowder's ninth season in 1971, CU was third in the nation at 10–2, behind only Big Eight rivals Nebraska (1) and Oklahoma (2). This was the first time that two teams from the same conference topped the final poll,[5] and it remains as the only time that a conference had the top three.
Crowder currently has the third best record as head coach at Colorado at 67–49–2 (.576). His teams went to five bowl games while he was head coach: the 1967 Bluebonnet (W), 1969 Liberty (W), 1970 Liberty (L), and 1971 Astro-Bluebonnet (W), 1972 Gator (L). He assumed the athletic director duties in 1965, retired from coaching in 1973, and hired his three replacements: Bill Mallory (1974–1978), Chuck Fairbanks (1978–1981), and most importantly, Bill McCartney (1982–1994), CU's all-time winningest coach at 93–55–5 (.624).