The Lions star was crowned Club Champion on Sunday night after polling 171 votes in a tightly contested count.
O’Dwyer finished six votes ahead of runner-up Belle Dawes, with Jennifer Dunne rounding out the top three on 160 votes.
It's been a memorable year personally for O'Dwyer, who also captained the inaugural Irish team in the Australia and Ireland match.
Lions AFLW senior coach Craig Starcevich praised O’Dwyer’s consistency and influence across the season.
“This is fitting recognition after an incredible year, from captaining Ireland at the beginning of the season to winning the Youi Fan MVP and now her first Club Champion award," Starcevich said.
“To become the first Irish player to win our AFLW Best and Fairest is a significant achievement, and one that will inspire the other Irish athletes in our group.
“Orla looked every bit like a leader on the field this season, and we're sure the experience of captaining her country played a role in this.
"She's finished on the podium twice before, placing second in 2021 and third in 2023, both times in premiership years.
“Orla is a much-loved teammate who has built strong relationships across the entire program.
“She is continually working on her growth areas and does everything on and off the field to get the best out of herself.”