The airfield was constructed by the Royal Canadian Air Force (RCAF) between 1940–1941 and was named RCAF Station Summerside.
It was home to No. 9 Service Flying Training School (SFTS), a flight school that operated under the British Commonwealth Air Training Plan. Relief or emergency airfields were located at nearby RCAF Station Mount Pleasant and Wellington. Airmen were trained on Harvards. In July 1942 No. 9 SFTS moved to RCAF Station Centralia and was replaced by No. 1 General Reconnaissance School (GRS) which flew Ansons. No. 1 GRS was changed to No. 1 Reconnaissance and Navigation School in 1945.
The station was closed in 1946 but reopened in 1947 with the formation of No. 1 Air Navigation School (ANS). This was a NATO training facility. No. 1 ANS left in 1953 and the Central Navigation School was established. In 1949 No. 2 (Maritime) Operational Training Unit started operation. The influx of personnel and their families required the building of more accommodation quarters. In 1949 the base housing was completed and named "Slemon Park" in honour of Air Marshal Roy Slemon.
During the Cold War, the base was home to anti-submarine and coastal patrol aircraft such as the Lancaster B.X, CP-122 Neptune, CP-107 Argus, and CP-121 Tracker. Other aircraft operated from Summerside include the CC-115 Buffalo and CH-113 Labrador. These aircraft were operated by various squadrons and units including No. 2 (Maritime) Operational Training Unit, No. 107 Rescue Unit, 413 Transport and Rescue Squadron, 420 Air Reserve Squadron, 880 Maritime Reconnaissance Squadron (Royal Canadian Navy), 31 Support Air Group (Royal Canadian Navy), and 415 Maritime Patrol Squadron.
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