City Parking ended the most recent financial year in the red after the value of the land used by thousands of motorists every day was found to be worth far less than was originally believed.
Its assets of the car parks were worth less than half as much as loans taken out against them, leaving the arms-length company deep in the red.
Graeme Hendry, leader of the opposition SNP group, claimed it was an example of council leader Gordon Matheson's financial mismanagement.
A Conservative councillor has called for full investigation.
Mr Hendry said Mr Matheson had "wasted millions" and left frontline services being cut to make up for his blunders.
He added: "It will be no surprise to find millions being lost on other crazy property deals."
But the council said the business, which has never turned a profit, was at "low" risk of defaulting on loans worth £27m more than its assets, the car parks.
And it stressed it still regarded the business as a going concern with a secure future.
Insiders admit the bald financial figures make grim reading and that the council is now effectively doomed to continue to foot the bill for a loss-making firm it can neither privatise nor take back into direct control.
City Parking's unaudited accounts show a loss on ordinary activities of £21.946m in the year through March 31, 2013. It made a loss of £1.029m in the previous 12 months.
The loss is being blamed on what council accountants called a "one-off £22m impairment" when its car parks were revalued last year.
The firm has lost more than £27m since it was created as an arm's length company by former council leader Steven Purcell in 2007.
A council spokesman said: "The value of car parks across the UK has been downgraded significantly in the last five years.
"City Parking is not immune to that and is effectively facing a negative equity situation.
"As many people who have experienced this domestically will understand; it only really has an impact if you intend to sell the property, which we don't. It has no cash effect on the business, which reported an operating surplus at year end, or on the council.
"City Parking's auditors have also confirmed the company is a going concern and is secure."
The company's financial problems date to its creation when it borrowed money to "buy" its car parks from its parent, the council, which in turn took the cash as a capital receipt.
City Parking has not raised enough income to make loan payments without incurring a loss as a result.
Opposition parties have been sceptical of the arm's length company model, which has since been adopted by Mr Matheson.
Conservative councillor David Meikle said: "There needs to be some kind of full-scale investigation into City Parking and its future, and this needs to involve councillors."
Spending watchdog Audit Scotland has been assured the council can cover City Parking's negative equity.