"I'm very sorry for any offence caused by what I said on the field during a heated encounter," Potgieter said in a statement.
"It was an offhand remark made without thought for the hurt it could cause to those around me."
Besides the fine, Potgieter will also be required to undergo additional education and awareness training.
ARU CEO Bill Pulver said Potgieter breached their code of conduct, which prohibited homophobic or racist comments.
He said the ARU inclusion policy was endorsed in August 2014, designed to stamp out all forms of discrimination and homophobia in the code.
"We take the issue of homophobia in sport seriously and want to provide a positive environment for everyone involved in rugby," Pulver said.
"Our inclusion policy reinforces Australian Rugby's commitment to ensure every individual, whether they're players, supporters, coaches or administrators, feel safe, welcome and included regardless of race, gender or sexuality.
"I'd like to stress again that there is absolutely no place for homophobia or any form of discrimination in our game and our actions and words on and off the field must reflect that."
Pulver said the sanction was determined in consultation with the Rugby Union Players' Association (RUPA) and the Waratahs and that the matter did not need to be heard by a tribunal because Potgieter accepted his penalty.
"Jacques made an error in judgment, despite having completed the ARU's integrity training, which includes the member protection policy around inclusion and racism," Waratahs CEO Greg Harris said.
"Our players have been educated around the importance of respect and integrity on the field, and this incident was directly in conflict to these values.
"There is no place for homophobia or any form of discrimination in our game and we have endeavoured as a club to embody these values on and off the field."
Pocock's allegations have the potential to not only further fuel the fierce Waratahs-Brumbies rivalry but also threaten to become an issue when players from the two squads come together on Wallabies duty in the coming months ahead of the World Cup.
Pocock has been an outspoken advocate for same-sex marriage, among other moral causes.
NSW Waratahs superstar Israel Folau said that was Pocock's business.
"Everyone's different," he said on Monday.
"I can't comment on the way he is as a person.
"That's not my place to say anything."