Abstract BACKGROUND Immune pathways are vital for insect vectors to combat viruses, yet arboviruses can evade this innate immunity, enabling persistent transmission. However, the mechanisms maintaining this immune homeostasis are still poorly understood. RESULTS This study thus aimed to decipher how the immune deficiency (IMD) pathway contends with rice gall dwarf virus (RGDV), a highly detrimental rice reovirus transmitted by leafhopper Recilia dorsalis . Notably, RGDV infection activated the peptidoglycan recognition protein 1 (PGRP1) upstream of the IMD pathway, which transmits signals to initiate the downstream Relish‐defensin1 cascade. Defensin1 is transcribed by the transcription factor Relish and serves as a broad‐spectrum antiviral peptide of the IMD pathway. Defensin1 promotes E3 ubiquitin ligase FBXW7‐mediated ubiquitination and degradation of viral tubular protein Pns11, inhibiting viral infection and transmission. However, the viral structural protein P8 hinders the nuclear translocation of Relish, thereby promoting the coexistence of arboviruses with their insect vectors. CONCLUSION The IMD pathway‐derived defensin1 mediates antiviral immunity in insect vectors. This study reveals a novel immune strategy in leafhoppers that confers resistance to rice viruses and elucidates an RGDV‐mediated mechanism for suppressing innate immunity. © 2026 Society of Chemical Industry.