Beginning his football career with Hawthorn in 1978, he had an illustrious career spanning from 1978–1993, playing 269 games and booting 70 goals.
He was part of a total of 5 premiership teams – 1983, 1986, 1988, 1989, and 1991. He won the Norm Smith Medal twice, adjudged best on ground in 1986 and 1988 and is one of only three players in the history of the AFL to do so.
Ayres captained Victoria against Tasmania in the 1989 State of Origin contest.
He captained the Hawks in his final two years from 1992–1993.
Gary played most of his football in defence, particular the back pocket position. He was nicknamed "Conan" by fans in reference to his powerful upper-body physique. He used his body to good effect in body on body contested situations. Ayres' height and weight was 187 cm / 100 kg. Allan Jeans described Ayres as "a good driver in heavy traffic"
After retiring, Ayres turned to coaching; starting as an assistant coach to Malcolm Blight at Geelong. After Blight's resignation in 1994 (following Geelong's Grand Final defeat to the Eagles), Ayres was appointed senior coach for the 1995 AFL season. In his first year, the Cats lost to Carlton in the Grand Final (their fourth Grand Final defeat in seven seasons) by 61 points. In 1999, at the end of a disappointing season (Geelong finished 11th) and following the Geelong board's refusal to offer him a contract extension beyond the 2000 AFL season, Ayres quit as Geelong coach to take the coaching position at Adelaide where Malcolm Blight had, again, just resigned.
Ayres coached Adelaide from 2000 until 2004. When told he would not continue as coach for the 2005 season, Ayres quit midseason. Though he had been given the opportunity to stay for the rest of Season 2004, he told the Adelaide board that if he could not coach the following year, he would leave immediately. He then walked out of the club's office without shaking hands or responding to media enquiries. He left Adelaide with a 55–52 win-loss ratio. He was replaced by Neil Craig, who coached for the remainder of Season 2004 and was eventually employed full-time.
When Matthew Knights was appointed as senior coach of Essendon at the end of the 2007 season, Knights vowed to modernise the club's support staff. Ayres subsequently lost his position as assistant coach and left to "pursue other football opportunities".
Victoria 19.12 (126) defeated Western Australia 10.12 (72), at the WACA Ground, 16 May 1989, crowd: 20,993 Victoria 22.17 (149) defeated South Australia 9.9 (63), at the MCG, 1 July 1989, crowd: 91,960