Pepper vein yellows virus (PeVYV, Luteovirdae; Polerovirus) infects Capsicum plants, whose bell pepper fruits (Capsicum annuum) are important crops in Japan. Reductions in the yield and quality of bell pepper fruits caused by PeVYV are agricultural problems in Okinawa Prefecture, Japan. The prevalence of PeVYV deposits in the annual disposition of harvested bell pepper plants suggests the possible existence of a reservoir for the virus. Here, we examined bird pepper plants (Capsicum frutescens) that were grown wild on five islands in Okinawa Prefecture, as well as cultivated peppers (C. annuum, Capsicum baccatum and C. frutescens) for the presence of PeVYV by reverse transcription polymerase reactions using specific primers. Overall, PeVYV was widely detected in bird peppers on the three islands (Okinawa, Miyako and Yonaguni) where the bell pepper disease occurred, but not detected in the plants from two islands (Ishigaki and Minami-Daito) with no disease. Laboratory experiments demonstrated that an Okinawa-derived strain of cotton aphid Aphis gossypii transmitted PeVYV from viruliferous wild bird peppers to the bell peppers, which may suggest an annual supply of PeVYV from wild bird peppers to the bell peppers via aphids in Okinawa Prefecture. Molecular phylogenetic analyses based on the nucleotide sequences of seven distinct genomic regions suggested that PeVYV detected from the bell peppers and bird peppers are indistinguishable, supporting the view that PeVYV moves frequently between these host plants.