Ray Flaherty played professional football with the Los Angeles Wildcats of the American Football League in 1926 and in the National Football League (NFL) with the New York Yankees (1927–1928) and New York Giants (1928–1935). He served as the head football coach at his alma mater, Gonzaga University, for one season in 1930. He was the head coach of the NFL's Boston/Washington Redskins from 1936 to 1942.

Ray put himself squarely on the spot in one of his first public utterances after being named head coach of the Boston Redskins in 1936. On hearing of the signing of Wayne Milner, Ray wired his boss, George Preston Marshall: "With that big Yankee playing end, please accept my resignation if we do not win the championship this year!"

History shows, however, that while the Redskins did not win, neither did Ray resign. Instead he stayed on with the Redskins, who moved to Washington in 1937, for six more years. In all, he led the team to two NFL championships and four divisional titles.  He guided the Redskins during the period that the Chicago Bears dominated pro football. Yet, his Redskins defeated the Bears two out of three times in NFL title showdowns.

Two important football innovations are credited to Ray and each played an important role in his two NFL championships.  In 1937, he introduced the behind-the-line screen pass against the Bears. Redskins quarterback Sammy Baugh threw three touchdown passes against the unprepared Chicago defenses for a 28-21 victory. Later, Ray developed a 1940s version of the two-platoon system. Both units played both ways but one unit emphasized the passing offense while the second platoon featured the ground game. This substitution plan was particularly effective in the 1942 championship year, his last season in Washington.

When Ray returned to civilian life after World War II, he opted to join the New York Yankees of the newly formed All-America Football Conference and there he won two straight divisional crowns. He closed out his coaching career in 1949 with the AAFC’s Chicago Hornets. For his entire coaching career, Ray's record shows 80 wins, 37 losses and five ties, for an excellent .676 lifetime winning percentage. He was inducted into the Pro Football Hall of Fame in 1976 for his contributions as a coach.  

After the end of the AAFC in 1949, Ray returned to the Spokane area to enter private business as a beverage distributor. During football season, he was a part-time columnist for the Spokane Daily Chronicle.

After an extended illness, Ray Flaherty died in 1994 in  Hayden, Idaho at the age of 90.