Kammala jumla mai zuwa: An fara kafa rundunar ne a watan Mayu na 1938 a matsayin Rundunar Sojojin Sama ta 12th, wani bangare na Brigade na Sojojin Sama na 69, a Yankin Sojan Kiev a filin jirgin sama na Kirovohrad daga 16th Separate Fighter Squadron. Da farko an sanye shi da Polikarpov I-16 da Polikarpov I-15bis. Ya yi yaƙi a cikin mamayewar Soviet na Poland, inda ya harbe jirgin saman Poland guda ɗaya. A watan Afrilu na 1940, Kyaftin Pavel Terentyevich Korobkov, Jarumin Tarayyar Soviet da kuma yakin basasar Spain, ya zama kwamandan rundunar. A watan Yuni, rundunar ta ba da tallafin iska ga
Harkokin Soviet na Bessarabia. A ranar 14 ga watan Yuli, an canza rundunar zuwa Rukunin Jirgin Sama na 15. Ya zama wani ɓangare na 64th Fighter Aviation Division a ranar 5 ga Janairu 1941. A ranar 22 ga Yuni, Laftanar Leonid Grigoryevich Butelin ya harbe wani Junkers Ju 88 kuma ya buge wani a kan Ivano-Frankivsk Airfield yayin da yake tashi a kan I-153, sojojin farko na farko na yakin. An kashe Butelin a cikin taran, wanda aka ba shi lambar yabo ta Red Banner. Rundunar ta yi yaƙi a yakin Kiev kuma an tura ta baya don sake sakewa. An canja shi zuwa 11th Reserve Fighter Aviation Regiment kuma an sake sanye shi da sabbin mayakan LaGG-3 a Rostov-on-Don a watan Oktoba. Ci gaban Jamusawa ya tilasta wa rundunar janyewa zuwa Kirovabad a Azerbaijan SSR don ci gaba da horo a watan Nuwamba. Bayan kammala sake kayan aiki, an tura rundunar zuwa Crimean Front a matsayin wani ɓangare na Rundunar Sojojin Sama ta 72 kuma ta yi yaƙi a cikin Tsaron Sevastopol. A ranar 26 ga Disamba, an sake sunan rukunin a matsayin 486th Fighter Aviation Regiment. A cikin kusan watanni shida na gwagwarmaya, 12th IAP ya yi 2607 sorties, ya harbe jirgin sama 75 kuma ya hallaka jirgin sama 97. Ya rasa jirage 61 kuma ya kashe matukan jirgi goma.