Wallabies captain Michael Hooper says the team will take a stand for marriage equality, joining the Football Federation, Cricket Australia and the NRL to support the 'yes' campaign.
The ARU unveiled a rainbow marriage equality logo on social media on Tuesday as a mark of the organisation's support as Australia braces for a marriage law postal survey.
It comes two years after former Wallabies captains David Pocock and Stephen Moore took an on-field stance against homophobia when a slur was used in a game between the ACT Brumbies and NSW Waratahs.
Pocock and Moore's decision to speak up sparked debate about sport's role in supporting and fighting against major issues in society, but the ARU was swift in issuing a $20,000 fine to Waratahs forward Jacques Potgieter.
Now the ARU and the entire Wallabies squad are throwing their weight behind what looms as a pivotal moment in Australian history.
"For a lot of guys, they're about footy and our job is rugby, but sport has ability to cross boundaries," Hooper said in Canberra.
"We're all very supported of the 'yes' campaign and this is the approach we've taken. I know guys at the Waratahs have done work with the Sydney Convicts [Australia's first gay rugby club].
"If that helps influence people, then fantastic. We're fully supportive of that and anything we can do."
FFA chief executive David Gallop confirmed the sport's long-running support for same-sex couples to marry on Tuesday and in doing so, the country's biggest participation sport joined rugby league, rugby union and cricket in united support..
"FFA is a founding member of Pride in Sport and supports its charter including marriage equality," an FFA spokesperson said.
"Everyone is welcome to be a part of the football community, regardless of their age, gender, sexual preference, ability or beliefs.
"David Gallop, CEO of FFA, was one of the first CEOs in the country to publicly support same-sex marriage over two years ago."
Australia's football governing organisations - AFL, NRL, ARU and FFA - have history supporting the cause, supporting a float at the 2015 Mardi Gras.
Players showed their intolerance for homophobia during the last A-League and W-League season, supporting the 'rainbow laces' campaign.
Sydney FC players also carried a rainbow flag to the pitch during a match timed alongside Mardi Gras in March as part of their inclusivity campaign.
Matildas and Canberra United striker Michelle Heyman was named sports personality of the year at the inaugural Australian LGBTI awards in March.
Her national team coach, Alen Stajcic, said he saw the round-ball code as a welcoming sport - irrespective of background or belief.
"Football has been the leader in Australia in giving people equality in all aspects of life," he told AAP.
"Whether it's sexuality or race or any different groups that we have in the country.
"Football has always been a leader in that space. I see it being a leader in this space in the future as well."
The postal survey, which asks Australians whether they support or oppose same- sex couples marrying, begins today. Responses will be collated in November.
- with AAP