Arthropod-borne viruses cause serious threats to human health and global agriculture by rapidly spreading via insect vectors. Southern rice black-streaked dwarf virus (SRBSDV) is the most damaging rice-infecting virus frequently transmitted by planthopper. However, the molecular mechanism underlying its propagation in the host and epidemic in the field is largely unknown. Here, we showed that SRBSDV-encoded P6 protein is a key effector regulating rice ethylene signaling to coordinate viral infection and transmission. In the early SRBSDV infection stage, P6 interacts with OsRTH2 in the cytoplasm to activate ethylene signaling and enhance SRBSDV proliferation, which also repels the insect vector to reduce infestation. In the late infection phase, P6 enters the nucleus where it interacts with OsEIL2, a key transcription factor of ethylene signaling. P6-OsEIL2 interaction tunes down ethylene signaling by preventing the dimerization of OsEIL2, which facilitates viral transmission by attracting insect vector. These findings unveil a novel molecular mechanism by which arbovirus orchestrates host defense system to benefit its infection and transmission.