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Castle brought to an end her tumultuous 2-1/2 year reign on Thursday night, handing in her resignation to RA chairman Paul McLean.
Completing one of the most brutal weeks in Australian sports management, Castle followed NRL boss Todd Greenberg out the door after a sustained attack on her leadership and an extraordinary call to arms from disgruntled former Wallabies captains.
A group of 10 former players, led by World Cup-winning captain Nick Farr-Jones, signed a letter calling for a change in RA's administration.
A horror final year in charge included a costly legal battle following the sacking of superstar Israel Folau, a poor World Cup performance and fractured relationship with then Wallabies coach Michael Cheika plus the failure to reach agreement for a broadcast deal.
The code is in dire financial straits, looking at a $120 million loss in revenue if no rugby is played this year due to the coronavirus pandemic.
Castle said in a statement that she had been told RA needed "clear air".
"I love rugby on every level and I will always love the code and the people I have had the honour of working with since I took this role," Castle said.
"I made it clear to the board that I would stand up and take the flak and do everything possible to serve everyone's best interests.
"In the last couple of hours, it has been made clear to me that the board believes my no longer being CEO would help give them the clear air they believe they need.
"The game is bigger than any one individual - so this evening I told the chair that I would resign from the role.
"I will do whatever is needed to ensure an orderly handover. I wish the code and everyone who loves rugby nothing but the best and I would like to thank the people I work with and the broader rugby community for their enormous support."
Former test hooker Phil Kearns, who was among the cohort to sign the captains' plea, missed out on the role to Castle just over two years ago.
He said he has the business experience and financial backing to get RA back on track and resurrect the Wallabies to their former glory after slumping to No7 in the world.
Castle met with Super Rugby chief executives on Thursday morning to plot their way through the competition shutdown and gave no hint she believed her time in the role was up.
She was however a late withdrawal from a meeting with the state chairmen to go over RA's financial position.
Castle completed an interview with ABC TV prior to her resignation and said then she believed David Rennie would honour his contract to coach the Wallabies regardless of her situation.
"Ultimately he knows that things can change and I know he has a desperate desire to coach the Wallabies. He's done a lot work and he's excited about the young talent coming through," she said.
"He will come here regardless of where I sit."