Nicola Sturgeon revealed plans for the Ayrshire airport, which was bought for £1 last year by the Scottish Government to prevent it closing with thousands of jobs at risk.
Ms Sturgeon said ministers would not show preference to Prestwick over any other airport and told MSPs there would be an arm's length company set up independent of government to run the day-to- day business.
She said the cash was in the form of loans and the plan was to return it to profitability, return it to private ownership and get a return for the tax payer's investment.
Ms Sturgeon said she couldn't put a timescale on when that would be, but it was long term.
She said: "We will be looking to make steady improvements across all the airport's activity. There is no quick fix. It will require sustained investment."
She said the aviation business for passengers and freight was less than half of the airport's income with other areas including repair and maintenance, land ownership and retail and parking.
Leaders of Glasgow and Renfrewshire councils were concerned about the impact on Glasgow Airport.
Gordon Matheson, leader of Glasgow City Council, said: "Glasgow Airport is vital to the economy of west central Scotland and its success is clear from the continued growth in passenger numbers.
"I have serious concerns about how the Scottish Government can justify using up to £15m of taxpayers' money to support an airport without a viable business case, while not contravening state aid rules.
"This has done nothing to reassure Glasgow that Government support for Prestwick will not jeopardise the success of Glasgow Airport."
Renfrewshire Council leader Mark Macmillan said there must be "fairness and transparency" in Government dealings with both airports.
He said: "The Scottish Government has a poor track record when it comes to maximising the economic, transport and investment potential of Glasgow Airport.
"It is essential that all the country's airports are treated fairly."