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He debuted for the Eagles in 1991 and played for the club in the centre half-back position and the number 27 guernsey. He was selected in that position in the All-Australian team of 1994 and 1995.
He was notable for his duels with rival centre half-forward, North Melbourne Football Club's Wayne Carey. Carey was considered to be one of the best of all time, and the contests between these two were highly anticipated events on the football calendar.
Jakovich also had a rivalry with Geelong Football Club All-Australian centre half-forward Barry Stoneham- Along with Carey this rivalry was highly anticipated when West Coast played Geelong.
After undergoing a knee reconstruction in 1996 he was unable to recapture his superlative form of the previous three years. Although still able to win his club's best and fairest award in 2000, he was not the imposing player of the past.
His brother Allen Jakovich was a full-forward for the Melbourne Football Club. During their career, the two brothers lined up against each other on more than one occasion. Another brother, Gary, had played with South Fremantle during the early 1980s. Glen was taller than his brother at 193 cm, but at 100 kg, both brothers were similarly solid in build.
Jackovich represented his state of Western Australia several times, in State of Origin. Jakovich has described that playing for his state, was one of his fondest memories in football. In 2003, Jakovich was selected as the Australia international rules football team's goalkeeper for the 2003 International Rules Series in Australia. Although the series was tied at one test win apiece, Australia won the series with a 101–94 aggregate score.
Glen Jakovich retired from football in 2004, kicking three goals in a win over Sydney Swans in his last game. Jakovich was the Eagles' games played record holder from 2003, when he overtook Guy McKenna's 267 games, until Dean Cox surpassed him in 2014.
Jakovich was an expert commentator on Fox Sports and 882 6PR, but now broadcasts from Western Australia for 1116 SEN Melbourne.