Gov. Andrew Cuomo announced the senate's confirmation Thursday night.
Since January, Prendergast had served as the MTA interim executive director. He succeeded Joseph Lhota, a Republican who resigned from the position to run for mayor.
Prendergast said in a statement the MTA faces challenges, such as improving service and rebuilding from Superstorm Sandy.
Prendergast has been CEO at TransLink in Vancouver, B.C., and began his career with the Chicago Transit Authority. He's also worked with the U.S. Department of Transportation.
He spent more than three years as president of MTA New York City Transit and six years as president of the Long Island Rail Road.