Potato virus Y (PVY) is an important plant pathogen with a wide host range that includes, among others, potato, tobacco, tomato and pepper. The coat protein (CP) of PVY has been commonly used in phylogenetic studies for strain classification. In this study, we used a pool of 292 CP sequences from isolates collected worldwide. After detecting and removing recombinant sequences, we applied Bayesian techniques to study the influence of geography and host species in CP population structure and dynamics. Finally, we performed selection and covariation analyses to identify specific amino acids involved in adaptation. Our results show that PVY CP diversification is significantly accounted for by both geographical and host-driven adaptations. Amino acid positions detected as positively selected concentrate in the N-terminal region of the protein. Some of these selected positions may discriminate among strains, and to a much lesser extent, between potato and non-potato isolates.