[3] Dempster played his first AFL game in Round 3, 2005, against the Brisbane Lions wearing guernsey number 26.

In the following AFL season, he played 18 matches, mostly as a defender, including the Sydney losing grand final team.

He played a total of 54 games for Sydney before being traded to the St Kilda Football Club with Adam Schneider at the end of the 2007 AFL season.

Dempster played in eight of the 22 matches in the 2009 season's home and away rounds in which St Kilda qualified in first position for the finals series, winning the club's third minor premiership.

The decision came as a result of a number of concussions Dempster suffered throughout his career, deciding it was too much of a risk to play football again and receive another blow to the head, having started a young family.