Ralston began his coaching career in 1953 at San Lorenzo High School in San Lorenzo, California, just south of Oakland. He subsequently was an assistant coach at Mt. Dioblo High School in Concord, Ca. in 1954 and 1955. He then spent three seasons as an assistant coach at Cal from 1956–1958.
Ralston turned down the head coaching job at Nebraska in 1962 before he moved to Stanford University in 1963 and helped revive a sagging program. Over nine seasons, Ralston guided the team back to national respectability while building a mark of 55–36–3. In his last two seasons, 1970–1971, Ralston's teams won two Pacific-8 titles and notched back-to-back Rose Bowl victories over Ohio State and Michigan, both of whom were undefeated coming into the Rose Bowl game. Under Ralston's tutelage, Stanford quarterbackJim Plunkett won the Heisman Trophy in 1970.
In 1972, Ralston departed the San Francisco Bay Area once again, this time for the Rocky Mountains and the Denver Broncos. The Broncos continue to struggle under Ralston finishing with a 5–9 record in 1972. In 1973, a year which included the "Orange Monday" game played in front of a prime-time national television audience in which the Broncos came from behind to earn a tie on Jim Turner's 35-yard field goal, Ralston coached the team into first place with a 6–3–2 record. With their first winning season in franchise history under their belt and with the AFC West title on the line, the Broncos season ended with a 21–17 loss to the Oakland Raiders. Ralston was the UPI's choice as AFC Coach of the Year after Denver achieved its first-ever winning season at 7–5–2.
In 1974, Ralston coached the Broncos to a 7–6–1 record for their second consecutive winning season. The 1975 season was one of mediocre play for the Broncos as the team finished with a disappointing 6–8 record, but the following year the team improved and finished with a 9–5 record. However, the record was not good enough qualify the Broncos for the playoffs. Despite the strong showing, Broncos players issued a protest vote of no confidence in their coach and Ralston resigned following the season. In five seasons with the Broncos, Ralston guided the team to winning seasons three times and an overall record of 34–33–3.
Ralston also coached in Europe. He was the head coach of the Dutch Lions, the national football team of the Netherlands. With the Lions, Ralston won the bronze medal in the European Championships in Helsinki, Finland in 1991.
After being inducted to the College Football Hall of Fame in 1992, Ralston came out of retirement in 1993 to be head coach at San Jose State University. After the 1996 season, Ralston resigned from the position to become special assistant to athletic director Tom Brennan. Ralston later became special assistant to the football team, where he would remain until the 2013 season.