It was formed on June 12, 1917, and was initially involved in construction duties, repairing war-damaged French villages, and working in salvage yards in France.

[3] The 35th Aero Squadron was moved to several different French aerodromes throughout 1917 and 1918, where they served in various non-combat capacities, such as assembling aircraft, maintaining vehicles, and ferrying pilots.

After two months in combat, the squadron rotated back to Australia, returning to Woodstock on 29 June 1942 for various rest and re-equipment tasks.

They relocated to Garbutt Field in Townsville on 27 July 1942 and then moved to Milne Bay in New Guinea on 18 September 1942 after the airfield was secured from the Japanese.

It again engaged in combat operations against Japanese forces with its P-39s until rotated back to Queensland, being sent to Mareeba Airfield in February 1943 as its Airacobras were basically worn-out.

At Mareeba, the squadron was re-equipped with Curtiss P-40N Warhawks before leaving Australia for good in May and heading back to Port Moresby.

In 1944, the 35th supported operations in the Philippines, earning a second Distinguished Unit Citation when, armed only with machine guns, the Lightnings of the 8th Fighter Group strafed a Japanese naval task force for three hours, halting the ships until North American B-25 Mitchell medium bombers from more distant bases could attack the task force with low-level bomb runs Despite the fact that the group did not have time to load bombs on its fighters and used only .50 caliber bullets on the mission, the 8th managed to sink one of the Japanese ships.

After moving to San Jose, Occidental Mindoro in the Philippines in December 1944, the 35th spent the next several months conducting offensive operations against Formosa and the Asian mainland, as well as flying escort missions in the area.

"[12] When the Korean War ended, the squadron started flying North American F-100 Super Sabres at its new location at Itazuke Air Base, Japan.

[12] In 1964, the 35th deployed to Korat Royal Thai Air Force Base, Thailand, as one of the first units to fight in Southeast Asia.