Dyer was born in Oakleigh, now a suburb of Melbourne, and grew up in Yarra Junction, a town on the Yarra River approximately 60 kilometres south-east of the city and played football there. Moving back to the city in 1927, he played amateur football before being invited to try out for the Richmond Tigers in 1931. He went on to play 312 games for Richmond, being voted the club's best and fairest player in 1932, 1937, 1938, 1939, 1940, and 1946. He played in seven Grand Finals for two premierships in 1934 and 1943, one as captain and playing coach of the side.
Dyer was a "ruckman", the 185 cm figure not particularly tall for the position even in that era. His on-field characteristics were summed-up in the nickname "Captain Blood", which he received from cartoonist John Ludlow in The Age in 1935, after the title character in an Errol Flynn Film. in an era where football was considerably rougher than today he was regarded as a "hard at the ball" player - a football euphemism for a player who is prepared to use strength, size, and momentum to simply run through and flatten an opponent to get the ball. This style of play was at least partly attributable to a knee injury that reduced his ability to make quick turns. Despite this reputation, he was reported only five times in a long career, and only suspended once. He was not simply a brute, however; as he gradually played more as a forward later in his career, he is credited with inventing the "drop punt", a kicking style that gradually gained popularity over the intervening decades and is now almost universal. He ended up kicking 443 goals, fifth on Richmond's list of all-time goalkickers.
Dyer represented Victoria in many interstate games.
Dyer retired from playing in 1949, and as coach in 1952.
During his football career, footballers held day jobs and Dyer had several jobs including serving in the police, and operating milk bars and hotels.
Dyer's achievements received recognition from his club and the AFL.The Tigers' best and fairest medallion was renamed the "Jack Dyer Medal". He is also one of the inaugural "AFL Legends" in the league's Hall of Fame (an award reserved for only a very few players).
After retiring from coaching, Dyer turned to the media, where he became a respected commentator and football media personality. He happily contributed to two tongue-in-cheek sports/comedy offerings on Melbourne television, World of Sport, a Sunday morning panel show, and later League Teams, a Thursday night variant which clearly inspired the current Footy Show.
Dyer also was a radio broadcaster - for many years he and Ian Major called football matches for radio station 3KZ (KZ-FM after the station converted to FM in 1990) as The Captain and The Major.
Not the most articulate on-air personality, Dyer's malapropisms became legendary. According to press orbituaries, he was responsible for such gems as "Yes, we had an enjoyable time on the French Riverina" (The Riverina is an area of southern New South Wales), and describing the problems with younger players by saying that "All they want to do is sit around and smoke marinara".
Retiring from the media in the late 1980s, Dyer had one last impact on the game, successfully leading a fight to save his club from a merger with St. Kilda.
Dyer married Sybil and had two children, Jackie and Jill.
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