Circular RNAs(circRNAs), a class of stable, covalently closed non-coding RNAs, are increasingly recognized for their diverse roles in cellular processes, including viral infections. Our previous study identified circRNA_vSP27, encoded by Bombyx mori cypovirus(BmCPV), which translates a micropeptide, v SP27, that activates the NF-κB-ROS signaling pathway, delaying viral replication.Here, we uncover additional mechanisms by which circRNA_vSP27 modulates BmCPV infection. We demonstrate that v SP27 induces autophagy, a critical cellular process for degrading damaged organelles and pathogens, through the NF-κB signaling pathway. This autophagy induction significantly inhibits BmCPV replication. In addition, circRNA_vSP27-bmo-miR-3339-TRSCH2 regulatory network is identified in BmN cells, which plays a pivotal role in suppressing viral replication. Specifically, circRNA_vSP27 acts by sponging the bmo-miR-3339, thereby influencing the expression levels of the TRSCH2 gene. Furthermore,we unveil a novel interaction between circRNA_vSP27 and hemolin-like protein, a key immune protein in Bombyx mori, further suppressing BmCPV replication.Our findings highlight the multifaceted nature of circRNA_vSP27's antiviral activity, encompassing both autophagy induction and interaction with host immune proteins. This complex regulatory mechanism emphasizes the critical role of viral-encoded circRNAs in shaping viral pathogenesis and offers exciting avenues for developing novel antiviral strategies.