Dyer was born in Oakleigh, now a south-eastern suburb of Melbourne, but grew up in the small farming hamlet of Yarra Junction on the Yarra River, approximately 60 kilometres (37 mi) east of the city. His parents, Ben and Nellie, were of Irish descent. The second of three children, Dyer had an elder brother, Vin, and a younger sister, Eileen. Dyer first played football at the Yarra Junction primary school. For his secondary education, Dyer was sent by his parents to St Ignatius in Richmond. He boarded in the city with an aunt. One of the brothers running the school offered Dyer a sporting scholarship to De La Salle College, Malvern. After leaving school with several sporting trophies, Dyer played with St Ignatius on Saturdays and with Richmond Hill Old Boys in a mid-week competition. Dyer's desire was to play for Richmond in the VFL as he admired one of the Tigers' players, George Rudolph.
In 1930, Dyer won the Metropolitan League's award for the best player at the age of 16. Richmond officials had not yet attempted to sign him, and Dyer applied for a clearance to play with the Tigers' main rival, Collingwood. The Richmond officials wanted to see him in action before any decision was made and Dyer was in training with Richmond for the start of the 1931 season. Richmond's coach 'Checker' Hughes pitting Dyer against veteran Joe Murdoch in a practice session. Dyer hardly touched the ball and was disheartened about his prospects until Hughes consoled him by explaining the pairing with Murdoch was a trial of courage, not skill.
Hughes selected him for his debut in just the second game of the season, against North Melbourne. Dyer was made a reserve while the team achieved a VFL record score of 30.19 (199) in one of the biggest wins in VFL/AFL history. Hughes left Dyer on the bench. It was the height of the Great Depression and the going rate for the players was 3 pounds per match, but Richmond only paid half that for unused reserves, so Hughes saved the club thirty shillings on the day. Dyer got another couple of chances and showed some form, but by mid-season found himself in the seconds team, with players who were not quite league standard, but wanted to stay on at the club and earn an extra few shillings per week to support their families.
At one point, Dyer walked away from Richmond for a few weeks and returned to suburban football. Club secretary Percy Page persuaded him back by promising to clear any recalcitrant players. In the run up to the finals, with Richmond sitting second on the ladder, ruckman Percy Bentley went down with an injury that ended his season. Hughes included Dyer in the Tigers' team for the second semi final against Geelong. Playing mainly up forward, the unknown Dyer played a successful game, kicking three goals. In the Grand Final a fortnight later, again against Geelong, Geelong used their player and coach "Bull" Coghlan playing on Dyer. Coghlan played roughly against Dyer; Dyer had only four touches for the day and admitted many years later to being intimidated.
The following year, partnering Bentley in the ruck, Dyer played successfully in the first half of the season before suffering a serious knee injury that put him out for the rest of the year. In ten matches, Dyer received four best afield Brownlow medal votes, collected enough votes to win the Tigers' best and fairest, although this is in dispute as there is no actual evidence that Dyer actually won the award, or even that there was one presented in 1932, and was chosen for Victoria after fewer than a dozen league matches. On Grand Final day, Dyer was back in reserve as his teammates won Richmond's third premiership after several finals failures.
Dyer did reappear in 1933, wearing a dirty knee bandage. In his own phrase, Dyer was unable to "turn off" or "pull up" and he sometimes collected a teammate if his timing was out. In the Grand Final against South Melbourne, Richmond lost by eight goals, but Dyer achieved thirty touches. In the following year's Grand Final, the Tigers won in a rematch with the Swans. Richmond's successfully used a ruck combination of Bentley, Dyer and rover Ray Martin.
The number of on-field incidents grew and after a particularly difficult game during 1935, newspaper cartoonist John Ludlow in The Age drew a picture of Dyer as a pirate and a journalist nicknamed him 'Captain Blood', after the Errol Flynn film Captain Blood. Initially, Dyer was angry at the connotation and the implied slur on his sportsmanship. Dyer preferred the 'hip and shoulder' method of meeting an opponent rather than grabbing him in a tackle. The force of being hit by the athletic, 89 kg frame of Dyer was often enough to leave a player prostrate and not wanting to re-enter the fray for a while. Occasionally, the hip and shoulder could go awry and Dyer's forearm would come into play, which was a reportable offence. In a nineteen-year career, he was reported five times and suspended once.
Dyer was keen to take on a coaching role, and had reportedly been promised the position of playing coach by the Richmond committee at the end of 1939 before it reneged and re-appointed Percy Bentley. As a consequence, Dyer announced that he would not play for Richmond in 1940. He received a lucrative offer to become captain-coach of the Yarraville Football Club in the Victorian Football Association (which, at the time, was aggressively recruiting VFL stars to play under its new throw-pass rules), and he lodged a request with Richmond for a clearance to the VFA club. Richmond rejected the clearance, and Dyer was unwilling to transfer without a clearance (even though one was not required at the time). Dyer ultimately decided to remain with Richmond as a player in 1940, and he was appointed captain-coach in 1941.
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; and, at 6'1" (185 cm), was not particularly tall for that position.
In 1947, Dyer crashed into Melbourne's Frank Hanna in round 15. The umpire cleared him for rough conduct, though Hanna was knocked unconscious. Don Cordner checked his pulse and Hanna was covered with a blanket, including his head, and was carried off on a stretcher. Dyer thought he had killed Hanna. By three-quarter time, he still believed he had killed him until he asked a Demon player about Hanna's condition, and Hanna had recovered.
He was selected as an interchange player in the AFL's 1996 Team of the Century"). He gradually played less as a ruckman and more as a forward later in his career. He invented the drop punt, a kicking style that gradually gained popularity over the intervening decades and is now almost universal, and has now spread to Rugby union, rugby league and American Football. He kicked 443 goals, fifth on Richmond's list of all-time goalkickers.
In 2009 The Australian nominated Dyer as one of the 25 greatest footballers never to win a Brownlow medal.
The "Jack Dyer Medal" is awarded each season to the winner of the Richmond Football Club's best and fairest count. Since the 2000s, the Richmond captain has automatically switched to wearing guernsey number 17, the number worn by Dyer throughout his career. But when Trent Cotchin took over the captaincy of the Tigers in 2013, he continued wearing his number 9.
After an assortment of jobs in his early adulthood, Dyer joined the police force in 1934. He married Sybil McCasker in 1939 at St Ignatius' Church, Richmond. Dyer served in the police for nine years, before becoming a publican in Port Melbourne, then later owned a milk bar.
On 8 March 1940, Richmond announced that they had refused the recently-married Dyer a clearance to coach VFA club Yarraville; and Dyer stated that he would not cross to Yarraville without a clearance.
He and his wife Sybil had two children, Jack junior (Jackie, born 15 December 1940) and Jill (married name Devine). Jackie had a brief career at Punt Road from 1959 to 1961, playing three games, but retired from all football aged just 23. Following Sybil's early death in 1967, Dyer met Dorothy Eskell with whom he spent 25 years. Dorothy supported him in his media career and they lived together in Frankston. In his final years Dyer went to a nursing home.
After retiring from coaching, Dyer turned to the media, where he became a commentator and football media personality. He contributed to two sports/comedy offerings on Melbourne television, World of Sport, a Sunday morning panel show, and later League Teams, a Thursday night variant which later inspired the current Footy Show. He also had a regular column which went under the name "Dyer 'ere" in Melbourne's Truth newspaper.
His media work began after resigning from the coaching position at Richmond. Dyer, along with former Collingwood captain Lou Richards, became an early television commentator on Australian football after the medium was introduced to Australia in 1956.
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.
According to press obituaries, Dyer was responsible for malapropisms including:"Yes, we had an enjoyable time on the French Riverina" (The Riverina is a highly productive agricultural region of south-western New South Wales) and describing the problems with younger players by saying that "All they want to do is sit around and smoke marinara".
Other moments include"I won't say anything in case I say something."
"Bartlett's older than he's ever been before."
"Johnston missed one from the 10-yard square – it was impossible to miss that."
"The only way to tackle Justin Madden. I don't know."
"That's the beauty of being small – your hands are close to your feet."
"Bamblett made a great debut last week, and an even better one today."
"The ball goes to Marceesie ... Marcheson ... McKann, er ..." before co-commentator Ian Major interjected: "Actually, Jack I don't think Marchesani was in that passage of play."
"Mark Lee's long arms reaching up like giant testicles."
"It's as dark out there as the Black Hole of Dakota."
"The goal posts are moving so fast I can't keep up with the play."
And on World Of Sport, Dyer declared that Fitzroy had "copulated to the opposition".
Retiring from the media in the early 1990s, when KZ-FM stopped broadcasting football, Dyer successfully led opposition to an AFL proposed merger of his old club with St Kilda in 1989.
A photograph was taken of Richmond captain-coach Dyer, aged 30 and playing his two hundred and twenty second game, wearing white strapping on his left thumb, and a dirty knee bandage on his left knee, breaking away from the pack, with his eyes fixed on the Lake end goals (Dyer went on to kick a goal), in the last quarter of the 1944 Preliminary Final, held at the Junction Oval, on Saturday 23 September 1944, in which Richmond defeated Essendon, primarily due to Dyer's nine goals.
Led by a four-goal burst by Dyer, who was playing at full forward — — Richmond scored 8.2 (50) to 0.5 (5) in the first quarter (kicking against the wind); and, although Essendon outscored Richmond in the last three quarters, Richmond won the match 16.12 (108) to 12.15 (87).
Dyer's performance that day was one of the best individual performances by a Richmond player in the club's history.
The photograph, which also appeared on the cover of the Australian Post's $4.50 booklet of ten "Richmond Tigers" postage stamps issued in 1996 as part of the "centenary of the AFL" celebrations, has also been the basis for:The logo of The Footy Show,
Mitch Mitchell's statue of Dyer at Punt Road Oval,
In 1996, the year the AFL celebrated the VFL/AFL centenary, it issued a set of four paintings by John Balmainof Ron Todd, Jack Dyer, John Coleman, and Alex Jesaulenko. All were taken from photographs; Dyer's was taken from the photograph of his break to score his ninth goal. It was also painted by Darcy Doyle, which was also used on the front cover of Brian Hansen's 1996 book.