The beginning of Oakland County International Airport occurred on September 12, 1928 with the purchase of 160 acres by the City of Pontiac. The airport opened on November 27, 1928 and was dedicated in June of 1929 by the Pontiac Junior Chamber of Commerce in memory of Harry Joseph Brooks, Oakland County's aviation pioneer.

The airport was part of the first Michigan Air Tour that took place June 10-16, 1929. The event was commemorated by a National Aeronautic Association of U.S.A. certificate signed by Orville Wright, Chairman of the Contest Committee.

On February 11, 1930 the airport received Certificate No. 000001, becoming the first in the nation to receive an A-1-A rating from the U.S. government.

The airport was transferred from the City of Pontiac to the County of Oakland on February 25, 1967. At the time the airport consisted of 482 acres. Most of the aircraft were owned by individuals, businesses and corporations in Oakland County, but few came from the City of Pontiac. The transfer thus reflected the fact that the airport already was functioning on a county-wide basis.

Oakland County International Airport ranks as the 118th busiest airport in the nation with 128,766 takeoffs and landings. It is ranked as the nation's thirteenth busiest general aviation airport and second to Detroit Metro in Michigan (2012 data).

Over 1/2 million passengers and pilots pass through the airport every year. More than 554 private and corporate aircraft are based here. In the course of a year virtually all the Fortune 500 companies use the airport.

The airport contributes over $175 million to the County's economy each year.

The aggregate tax contribution of airport businesses ranks the OCIA community the second highest taxpayer in Waterford Township.

Customs service became available on a limited basis in January 1990 and on a fulltime daily basis on January 2, 1996.

On March 7, 1996 the Oakland County Board of Commissioners renamed the facility Oakland County International Airport.

A "green" terminal building was completed in 2011.