He will be replaced by former Jetstar boss Jayne Hrdlicka.
"I appreciate Virgin Australia's unique culture and I want to protect and build on it ... and I am determined that Virgin Australia reinvigorates its strong brand and its passion for customer service while embracing the diversity, talent and strength of its people", she said.
She previously held the role of chief executive officer at Jetstar.
When it was forced into voluntary administration in April, the airline's woes attracted a pack of private equity firms and other parties keen to acquire the airline before Bain Capital came out on top.
On Wednesday, the TWU suspended enterprise negotiations with Virgin after increasing speculation about Ms Hrdlicka's appointment. "It will result in the loss of many more jobs and could herald the demise of Virgin", it warned.
The state government, which invested $200m for a 7 per cent stake in the airline, said it was not privy to management discussions.
Virgin's administrators from Deloitte confirmed the resignation in a statement to ASX on Thursday.
Mr Scurrah's 18-month stint as Virgin boss is the shortest of its three CEOs. But that came at the cost of years of losses. On April 20, with its cash reserves of $1bn dwindling, Virgin announced to the stock market that it had collapsed into administration with nearly $7bn in debt.