The unfolded protein response (UPR) is a vital cellular pathway that maintains endoplasmic reticulum (ER) homeostasis under conditions of ER stress and is associated with the degradation of misfolded proteins. However, the role of ER-associated degradation in plant-microbe interactions has yet to be explored. In this study, we identified a novel viral protein, βV1, encoded by the tomato yellow leaf curl betasatellite (TYLCCNB), which is localized to the ER and triggers ER aggregation. Transient expression of βV1 in Nicotiana benthamiana induces robust ER stress and activates the bZIP17/28 branch of the UPR signaling pathway. The induction of bZIP17/28 by βV1 is crucial for successful virus infection. Furthermore, we demonstrated that βV1 is unstable in N. benthamiana mesophyll cells, as it is targeted for autophagic degradation. The autophagy-related protein ATG18a, a key component of autophagosomes, participates in the degradation of βV1, thereby exerting an anti-viral role. Taken together, our results reveal a novel function of the βV1 protein and provide the first evidence for involvement of bZIP17/28 and ATG18a in ER-associated autophagic degradation during geminivirus infection. These findings significantly expand our understanding of the arms-race dynamics between plants and viruses.