The South Ayrshire site, which was rescued by the Scottish Government in 2013 for Â£1, will take until 2032 to refund nearly Â£40 million it has borrowed to stay in business.
Finance and commercial director Derek Banks told Holyrood's rural affairs and connectivity committee that repayments were not expected to start until 2022.
That is when the airport is projected to break even and return to private ownership, but the payments were expected to take ten years to complete.
He admitted the airport's current value was "very low" but declined to provide a figure.
Mr Banks also said the value did not take into account Â£12m spent on upgrading work since the airport was taken into state hands.
Chairman Andrew Miller said the airport had "lacked significant investment under the previous owners".
When asked if the airport would be able to repay the Â£39.6m loan, Mr Banks said: "We believe it is going to be possible".
However, Liberal Democrat Mike Rumbles said: "I'm not confident we are going to get our money back."
Mr Banks said the airport was still making losses, but they were reducing, and its performance over the last two years had been "better than expected".
He said income from military flights had increased by 37 per cent, and spare property was now 95 per cent occupied compared to 58 per cent previously.
However, he admitted cargo was "still a struggle", although the airport had handled five Boeing 747 jumbo jet freighters carrying costumes for a two-night show at the Hydro arena in Glasgow.
Passenger numbers - which contribute one third of income - fell from 1.1m a year to 624,000 in 2014.
But they increased to 678,000 last year and are expected to grow to 710,000 this year.
Chief executive Ron Smith told the committee the fall had prompted the airport to publish a new strategic plan.
He said: "I would characterise it as the patient was bleeding and we needed to stabilise the patient.
Mr Smith said the airport was striving to expand from Ryanair as its sole passenger operator.
He said there were "a number of very strong possibilities from new airlines and routes."
Among these, a London link was "our prime focus".
He said: "We are working tirelessly with a number of airports in London to set that up."
Mr Smith said other airports were running out of capacity, and airlines might not be able to get a time slot at Edinburgh - Scotland's busiest - at a time they wanted.
The chief executive said Prestwick was also "far closer to Ryanair than we have ever been", and they were discussing further expanding the airline's aircraft maintenance base there, which already employs around 300 people - a similar number as the airport itself.
Ryanair also announced a new route to Rzeszow in Poland last month - the airport's first brand new link for three years.