The squadron activated on 16 June 1952 at Biggs Air Force Base, Texas.
 However it was minimally manned until September 1953, when it began strategic bombardment training with Convair B-36 Peacemakers.
It operated in support of Strategic Air Command (SAC)'s global commitments beginning in April 1954.
The squadron deployed with the entire 95th Bombardment Wing to Andersen Air Force Base, Guam from July to November 1955.

From 1959 to 1960, the 95th wing phased out its B-36 and received Boeing B-52 Stratofortresses to replace them.
 In the late 1950s, SAC established strategic wings to disperse its B-52s over a larger number of bases, thus making it more difficult for the Soviet Union to knock out the entire fleet with a surprise first strike.
As part of this program, the squadron moved to Bergstrom Air Force Base, Texas on 15 January 1959, where it was assigned to the 4130th Strategic Wing.

Starting in 1960, one third of the squadron's aircraft were maintained on fifteen-minute alert, fully fueled, armed and ready for combat to reduce vulnerability to a Soviet missile strike.
 This was increased to half the squadron's aircraft in 1962.
The 335th continued to maintain an alert commitment until it was inactivated.

In February 1963, The 340th Bombardment Wing moved on paper from Whiteman Air Force Base.
Missouri and assumed the aircraft, personnel and equipment of the discontinued 4130th wing.
The 4130th was a Major Command controlled (MAJCON) wing, which could not carry a permanent history or lineage, and SAC wanted to replace it with a permanent unit.
 The 335th was inactivated and its mission, personnel and equipment were transferred to the 340th wing's 486th Bombardment Squadron.
The squadron activated on 16 June 1952 at Biggs Air Force Base, Texas.  However it was minimally manned until September 1953, when it began strategic bombardment training with Convair B-36 Peacemakers. It operated in support of Strategic Air Command (SAC)'s global commitments beginning in April 1954. The squadron deployed with the entire 95th Bombardment Wing to Andersen Air Force Base, Guam from July to November 1955.
From 1959 to 1960, the 95th wing phased out its B-36 and received Boeing B-52 Stratofortresses to replace them.  In the late 1950s, SAC established strategic wings to disperse its B-52s over a larger number of bases, thus making it more difficult for the Soviet Union to knock out the entire fleet with a surprise first strike. As part of this program, the squadron moved to Bergstrom Air Force Base, Texas on 15 January 1959, where it was assigned to the 4130th Strategic Wing.
Starting in 1960, one third of the squadron's aircraft were maintained on fifteen-minute alert, fully fueled, armed and ready for combat to reduce vulnerability to a Soviet missile strike.  This was increased to half the squadron's aircraft in 1962. The 335th continued to maintain an alert commitment until it was inactivated.
In February 1963, The 340th Bombardment Wing moved on paper from Whiteman Air Force Base. Missouri and assumed the aircraft, personnel and equipment of the discontinued 4130th wing. The 4130th was a Major Command controlled (MAJCON) wing, which could not carry a permanent history or lineage, and SAC wanted to replace it with a permanent unit.  The 335th was inactivated and its mission, personnel and equipment were transferred to the 340th wing's 486th Bombardment Squadron.
335th Bombardment Squadron