They include former communications chief of the Glasgow 2014 Commonwealth Games, Gordon Arthur, and former Port of Dover chief executive Bob Goldfield.
The Scottish government bought the struggling airport for £1 in 2013 amid fears it would be forced to close.
It is now being operated under public ownership "on a commercial basis".
The other new appointments to the board are Jayne Maclennan, a group director at transport giant FirstGroup, and Ken Dalton, a former senior executive at professional and technical services firm Aecom Technology Corporation.
Prestwick Airport said the appointments were the latest step in "the process of transforming the business into a successful and vibrant airport".
Airport chairman Andrew Miller said: "I firmly believe the airport has a bright future and it's my team's priority to see it return to profitability and become a strategic anchor for economic growth in Ayrshire and Scotland."
Scottish Infrastructure Secretary Keith Brown said: "This is another important step forward for the future of Glasgow Prestwick Airport, and I welcome the appointment of the four non-executive directors.
"We know there is real potential for growth at Glasgow Prestwick Airport, but it will take strong leadership and vision to drive this improvement and transform the airport into the successful and vibrant business we know it can be."
The airport had a pre-tax loss of £9.77m in its final full year under previous owners Infratil.
Last year, then Deputy First Minister Nicola Sturgeon warned there was "no quick fix solution for Prestwick" and the airport may not be profitable for several years.
Efforts to revive the fortunes of Glasgow Prestwick Airport have been stepped up with the appointment of four non-executive directors to its board.