When Ewbank was hired as head coach of the Baltimore Colts in 1954, Winner went along and helped the team capture NFL titles in both 1958 and 1959. At the conclusion of the 1962 NFL season, Ewbank was dismissed, but Winner stayed under new coach Don Shula from 1963 to 1965.
On February 10, 1966, Winner was hired as head coach of the St. Louis Cardinals. In five seasons at the helm, Winner managed a 35-30-5 record, but after failing to reach the postseason, was fired on January 6, 1971.
The Cardinals posted winning records in three of Winner's five seasons with the Cardinals, but fell achingly short of the playoffs each time. In 1966, the Cardinals started out 5-0 but lost four of their last five games to finish at 8-5-1 and in fourth place in the NFL East. In 1968, St. Louis finished one-half game behind the Cleveland Browns (9-4-1 to 10-4) in the NFL Century Division despite sweeping both regular-season meetings with the Browns. In 1970, St. Louis rolled to an 8-2-1 record at the end of November, including three consecutive shutouts over the Houston Oilers (44-0), Boston Patriots (31-0) and Dallas Cowboys (38-0 on Monday Night Football in Dallas). But with the NFC East championship in sight, the Cardinals stumbled in December, losing to the Detroit Lions, New York Giants and Washington Redskins to finish at 8-5-1 and in third place in the division behind Dallas and the Giants.
Winner wasn't out of work long, as he was soon hired by George Allen of the Washington Redskins. Winner worked two years for the Redskins, helping them reach the NFL playoffs during each season and their first Super Bowl berth ever in 1972. On February 1, 1973, he rejoined Ewbank as an assistant with the Jets and was also designated his successor following the end of the 1973 NFL season. Winner struggled to achieve success with the Jets, finishing 7-7 in 1974, needing to win the season's final six games to reach the .500 mark. The following year saw the team win only two of the first nine games, a decline that resulted in his dismissal on November 19, three days after a 52-19 loss to the Colts.
Two months later, Winner was hired as an assistant with the Cincinnati Bengals, spending the next four years with the team before once again being fired following the 1979 NFL season. Renewing acquaintances with Don Shula in 1981, Winner was hired to serve as player personnel director for the Miami Dolphins. He spent two years in that role before shifting to pro personnel, performing many of the same duties as a general manager, especially negotiating player contracts. On June 1, 1992, he announced his retirement.