The squadron served in the final stages of World War II, seeing combat operations in the Western Pacific from May 1945 to August 1946 while it was stationed in the Ryukyu Islands, first on Ie Shima and later on Okinawa.

The 34th Tactical Fighter Squadron performed strike missions in support of a recovery operation for the SS Mayagüez, a merchant freighter captured by Cambodian Khmer Rouge guerrillas in May 1975.

[5] On 23 December 1975, the 34th, as part of the 388th Tactical Fighter Wing, was relocated to Hill Air Force Base, Utah, still flying the F-4D Phantom II.

For the next several years, the squadron conducted initial qualification training for pilots from around the world, including those from Belgium, Denmark, the Netherlands, Israel, and Norway.

[5] When Iraq invaded Kuwait in August 1990, the 34th found itself backing up the front-line forces of the 388th Tactical Fighter Wing (Provisional) in Southwest Asia for Operation Desert Storm.

In June 2000, the 34th was the first active duty squadron deployed to Curaçao, Netherlands Antilles in support of Operation Coronet Nighthawk, flying drug interdiction missions in Latin America.

[2] The 34th was activated on 17 July 2015 with plans for it to become the first combat squadron of the 388th Fighter Wing (and the first in the U.S. Air Force) to receive the Lockheed Martin F-35A Lightning II.