The 'Rapiers' were raised on 10 August 1958, becoming the fourth unit to operate Canberra B(I) 58 in the IAF. Raised under the command of Wg Cdr NB Naik at Pune, the squadron first went into action in 1961. It's aircraft took part in the attack to disable Dabolim airfield in Portuguese held Goa. No.35 Sqn's Canberras were first moved north during the confrontation with China. In the event that no air action was authorized during the conflict in November 1962, no combat sorties were flown by any Canberra units.

The squadron's first sustained combat operations occurred during war against Pakistan in 1965. The squadron, then based at Halwara under Wg Cdr Bakshish Singh, went on alert in late August 1965. Over a ten day period, beginning 01 September 1965. The squadron flew 69 operational sorties. The most intense missions against Kasur and Sargodha being flown between 7th and 10th September. Although the Squadron flew with distinction (Sqn Ldr JP Gupta earning a Mention-in-Despatches for bombing Kasur), a spate of accidents caused the unit to be withdrawn from action after 10 September 1965.

A pilot gets ready to take-off from a EW-equipped MiG-21M at Bareilly AFS

The war in 1971 provided this young squadron an opportunity to perform to its full potential. During the war, No.35 Sqn's Canberras flew day and night missions on both fronts. A total of 92 operational sorties amounting to 900 hours were undertaken by the squadron during the conflict. The highlight of war was its bombing of the oil refinery at Karachi - resulting in, according to a recce pilot, "the biggest blaze ever seen over South Asia." While the squadron lost an aircraft and two pilots (Flt Lt SC Sandal and Flt Lt KS Nanda) over Karachi, the raid earned Wg Cdr KK Badhwar a Vir Chakra. Over the course of the conflict the squadron earned one Ati Vishisht Seva Medal, five Vir Chakras, six Vishisht Seva Medals, one Vayu Sena Medal and three Mention-in-Despatches. The Squadron went on alert during Operation Safedsagar in the summer of 1999. The squadron deployed a flight each to support offensive and defensive operations by Western and South Western Air Command (SWAC). No.35 Sqn's aircraft deployed to bases in Kashmir as well as to  the Rann of Kutch.