The airport was formerly a military field, established in 1940 as RCAF Station Summerside, changing its name to CFB Summerside in 1968. The base was active in training aircrews in the British Commonwealth Air Training Plan during World War II and hosting search and rescue (SAR) and coastal surveillance units during the Cold War. It was closed in 1990 and transferred to a local development authority named Slemon Park Corporation. The base property is now referred to as Slemon Park and the airfield has been named Summerside Airport. The airport is home to several aircraft maintenance companies, as well as a small general aviation community.
The Summerside Airport's airfield and terminal facilities are located in the township of Lot 17 and not in the city of Summerside proper; the municipal boundary is adjacent to the airport property with the city including the residential area of Slemon Park but not the airfield and industrial properties.