Transmission from host to host is a crucial step in the life cycle of pathogens, particularly of viruses, ensuring spread and maintenance in host populations. The immobile nature of plants and the strong pectin and cellulose barrier surrounding cells have constrained most plant virus species to use vectors (mainly insects) for exit, transfer and entry from one host to another. A growing body of evidence is showing that plant viruses can influence vector physiology and behaviour to increase their chances of transmission, either directly or through modification of the host plant. In contrast, little is known on the possible reciprocal interaction, where the vector way of life would significantly impact on the viral behaviour and/or phenotype within the infected plants, on its population genetics and its evolution. The complex possible reaches of these three-way interactions on the ecology of each partner have not been exhaustively explored. After briefly summarizing the current knowledge on how viruses can induce changes in insect vector behaviour, physiology and population dynamics, this review focuses on presenting unforeseen aspects related to (i) the impacts that the feeding habits of different insect vectors can have on the evolution of plant viruses and (ii) the possibility that vector-related stresses induce major switches in the 'behaviour' of viruses in planta, affecting primarily the efficiency of transmission by insect vectors.