The second-year Geelong midfielder kicked the Cats' only goals - including the match winner with less than a minute left - as they beat Richmond on Sunday by four points.
Geelong won 2.3 (15) to 1.5. (11) despite ideal football conditions on Sunday at GMHBA Stadium.
Richmond coach Ryan Ferguson said the two teams failed to adjust to the fierce pressure of the match.
"It was really hard, tough footy, but obviously both teams weren't able to take their moments, to get out and then execute," he said.
"We can handle the pressure better and execute better - and Geelong would probably say the same thing.
"We have more attacking flair that we can produce, but understand this was a red-hot game of footy."
Prespakis, the No.2 pick in the 2021 draft, kicked her first AFLW goal with a snap in the third term after Richmond looked set to take control of the game.
Then with less than a minute left, she was awarded a contentious free kick about 35m from goal because of a tackle from Monique Conti.
The ease with which Prespakis kicked the match-winning goal was in stark contrast to the rest of the game.
"To have repeat entries was really positive for us and for Prespakis to take her moment was something she built from last year, it's exciting for the club," said Cats coach Dan Lowther.
Richmond were left rueing four behinds in the second term, all from gettable set shots.
The Tigers will also sweat on the match review, with Beth Lynch in trouble for a first-quarter tackle on Geelong's Rachel Kearns, who suffered a shoulder injury which sidelined her for the rest of the game.
"We're all hopeful it's not surgery," Lowther said.
Courtney Wakefield kicked Richmond's only goal in the first term.
Richmond finished 11th last season, one place higher than Geelong, and the two sides will struggle to break into the finals again this season unless they can dramatically boost their forward firepower.
Prespakis impressed with 16 disposals and eight tackles, while captain Meg McDonald was rock-solid in defence.
Richmond defender Eilish Sheerin was outstanding in her AFLW debut, racking up 19 disposals and five marks.
Sheerin looked to have made a game-saving tackle late in the last quarter in the Geelong goal line, only for Prespakis to be awarded her decisive free kick moments later.
Richmond's acting skipper Sarah Hosking had a team-high 22 disposals. Regular captain Katie Brennan did not recover from her off-season foot surgery in time to take part.
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