The airport land was originally a military rifle range. In 1918, the Royal Air Force began using the field behind the range for experimental mail flights, and the airport opened officially in 1920 as the Ottawa Air Station, one of the six original airfields opened across Canada by the new Air Board. Since it is on the shore of the Ottawa River and the runways were connected to the riverfront by a road, it was one of very few airports capable of handling and transferring floatplanes on both land and water. On March 12, 1930, Canadian World War I flying ace William George Barker crashed into the Ottawa River and died during an aerial demonstration over the field. In July 1931, Charles Lindbergh and Anne Morrow Lindbergh visited the airport during their northern surveying tour. During World War II. Rockcliffe participated in the British Commonwealth Air Training Plan and many other kinds of testing, training, and transport operations, including flying overseas mail to troops in Europe.

The military importance of the airport declined after World War II, since the runways were too short for typical jet operations. The armed forces shifted most operations to RCAF Station Uplands (now Ottawa Macdonald–Cartier International Airport) in 1957, and ceased flying operations at Rockcliffe in 1964, retaining the station only as an administrative base, while the Rockcliffe Flying Club began using the field for civilian flying.

During the 1970s, the airport was also used for scheduled short takeoff and landing (STOL) commercial flights to the short-lived Victoria STOLport near downtown Montreal. The objective was to demonstrate Twin Otter STOL aircraft in downtown areas and avoid longer drives to the Ottawa Macdonald–Cartier and Montréal–Trudeau airports. For a variety of reasons STOL operations in downtown settings have not proven successful.

The military left the airport completely in 1994, but their aircraft collection remained to form the nucleus of the Canada Aviation and Space Museum. Only one of the former triangle of runways remains active. Runways 04/22 and 15/33 were closed along with most taxiways now servicing the aviation museum.