Persistent, non-propagative vector-borne plant viruses are mostly transmitted by whiteflies and aphids. Specificity and co-evolution of viruses with their respective insect vectors ensures mutually exclusive transmission of viruses only from specific group, either by a whitefly or an aphid, and not the two, despite the high similarity in the circulative transmission routes of these viruses within the insect. The insect and viral genetic elements determining specific transmissibility are highly conserved and impedes evolution of new virus-vector relationships. However, co-existence of two poleroviruses infecting pepper crops in Israel: Pepper vein yellows virus 2 (PeVYV-2) and Pepper whitefly-borne vein yellows virus (PeWBVYV) which share high genetic identity has been recently reported. PeWBVYV is unusually transmitted by the Middle East Asia Minor 1 (MEAM1) species of the whitefly Bemisia tabaci (B. tabaci) and not aphids, which were the only known vectors for poleroviruses. The effect of co-infection by these two discretely transmitted viruses inside the host plant and insect vector on virus titers and transmission compared to single infections revealed a competitive nature of interactions between these viruses. The aphid transmitted PeVYV-2 was the dominant strain within the host plant whereas, the whitefly transmitted PeWBVYV was the stronger competitor inside the insect vector. Moreover, PeWBVYV required much higher circulation time inside the whitefly compared to PeVYV-2 in aphids before transmission. Furthermore, PeWBVYV was only transmissible by MEAM1 and not by the Mediterranean (MED), the other prevalent species of B. tabaci in Israel.