Plant viruses pose serious threats to stable crop yield. The majority of them are transmitted by insects, which cause secondary damage to the plant host from the herbivore-vector’s infestation. What is worse, a successful plant virus evolves multiple strategies to manipulate host defenses to promote the population of the insect vector and thereby furthers the disease pandemic. Jasmonate (JA) and its derivatives (JAs) are lipid-based phytohormones with similar structures to animal prostaglandins, conferring plant defenses against various biotic and abiotic challenges, especially pathogens and herbivores. For survival, plant viruses and herbivores have evolved strategies to convergently target JA signaling. Here, we review the roles of JA signaling in the tripartite interactions among plant, virus, and insect vectors, with a focus on the molecular and biochemical mechanisms that drive vector-borne plant viral diseases. This knowledge is essential for the further design and development of effective strategies to protect viral damages, thereby increasing crop yield and food security.