Avian leukosis virus subgroup J (ALV-J) is an immunosuppressive neoplastic virus, the growth retardation and growth performance of chickens after infection. Circular RNAs (circRNAs) play a crucial role in various types of cancer. In a previous study, we showed that circ-Vav3 was significantly elevated in the tumor livers of avian leukosis-infected chickens. Autophagy is an essential cellular process, and circRNAs have been confirmed to be key players in autophagy regulation. In this study, we demonstrated that overexpression of circ-Vav3 inhibited autophagy. Specifically, circ-Vav3 functions as a sponge for gga-miR-375, resulting in increased expression of CIP2A, which is a target gene of gga-miR-375. CIP2A, in turn, hinders the fusion of autophagosomes with lysosomes, leading to incomplete autophagic flux, consequently, the inhibition of autophagy. Further study confirmed that overexpression of gga-miR-375 inhibits CIP2A expression and promotes autophagy by downregulating p-AKT. Additionally, we treated cells with rapamycin to induce autophagy and then cotransfected them with circ-Vav3 and gga-miR-375. The results demonstrated that cotransfection of circ-Vav3 and gga-miR-375 inhibited cellular autophagy. Moreover, cells cotransfected with circ-Vav3 and gga-miR-375 exhibited further autophagy inhibition after ALV-J infection, suggesting that circ-Vav3 is involved in inhibiting autophagy caused by ALV-J infection through the regulation of gga-miR-375/CIP2A/AKT. In conclusion, our results demonstrated that circ-Vav3 inhibited autophagy through the gga-miR-375/CIP2A/AKT pathway and mediated the suppression of ALV-J-induced autophagy.