Holmes moved to Darwin in the Northern Territory with her partner, Nathan Brown, in 2012 so that Brown, who had previously played in the South Australian National Football League for West Adelaide and North Adelaide, could play in the Northern Territory Football League (NTFL) during the summer (most Australian rules leagues are played in winter). Holmes had planned to continue playing netball in Darwin, but she also began playing football for Waratah Football Club in the women’s competition of the NTFL. She played football in the summer and netball in the winter, as the seasons did not overlap. Holmes immediately had success in the NTFL. In her first four seasons, she was both the league’s leading goalkicker and a premiership player with Waratah, becoming one of the highest-profile female footballers in the Northern Territory.

In 2014, Holmes became the first woman to kick 100 goals in a season in an established women’s football league, kicking 105 goals across 15 games in the 2013–14 NTFL season. She kicked seven or more goals in a single match on nine occasions and kicked ten or more thrice, including kicking 16 goals and five behinds in a match against Tracy Village. As a result of her achievement, she was mentioned by name in Federal Parliament.

Holmes’ success in the NTFL led to her being selected to play in various exhibition matches. She played in a West End Slowdown, sharing player-of-the-match honours with Adelaide legend Andrew McLeod and played in two E. J. Whitten Legends Games. Despite this, she was consistently overlooked by the Melbourne Football Club and the Western Bulldogs, who played annual exhibition matches. After missing out on the 2014 match, she asked then-Melbourne coach Michelle Cowan what she needed to do to improve her game and she was told that her game was too one-dimensional. Rather than staying at full-forward she needed to be able to help her team further up the field, so she started to work on this.

During the 2016 NTFL Grand Final, in which Holmes won her fourth consecutive premiership, she suffered torn rib cartilage. The nature of the injury meant there was no rehabilitation beyond just resting and waiting for it to heal. In 2016, she played two exhibition matches representing the Northern Territory, but in both matches she re-tore the cartilage. She was meant to play for the St Kilda Sharks in the Victorian Women’s Football League in the 2016 season, but the recurring injury meant she was unable to do anything beyond train. Instead, Holmes started to work for the Seven Network as the boundary rider for their coverage of the Victorian Football League. At the end of the year she also presented the Goal of the Year award to Adelaide player Eddie Betts.

Holmes was drafted by the Adelaide Football Club with their thirteenth selection and 103rd overall in the 2016 AFL Women’s draft, the team she had been supporting for her entire life. Going into the inaugural 2017 AFL Women’s season, she was expected to be one of Adelaide’s star players, but for the first match of the season she wasn’t initially selected to play, only being listed as an emergency replacement. She was a late inclusion into the team and made her debut in the thirty-six point win against Greater Western Sydney at Thebarton Oval.

Adelaide re-signed Holmes for the 2018 season during the trade period in May 2017. She was delisted by Adelaide at the end of the 2018 season.