Sweet potato feathery mottle virus (SPFMV, genus Potyvirus) is globally the most common pathogen of cultivated sweetpotatoes (Ipomoea batatas; Convolvulaceae). Although >100 SPFMV isolates have been sequence-characterized from cultivated sweetpotatos across the world, little is known about SPFMV isolates from wild hosts and the evolutionary forces shaping SPFMV population structures. In this study, forty-six SPFMV isolates from 14 wild species of genera Ipomoea, Hewittia, and Lepistemon (barcoded for the matK gene) and 13 isolates from cultivated sweetpotatoes were partially sequenced. Wild plants were infected with the EA, C, or O strain, or co-infected with the EA and C strains of SPFMV. In East Africa, SPFMV populations in wild species and sweetpotato were genetically undifferentiated, suggesting inter-host transmission of SPFMV. Globally, spatial diversification of the 178 isolates analyzed was observed, strain EA being largely geographically restricted to East Africa. Recombination was frequently detected in the 6K2-VPg-NIaPro region of the EA strain, demonstrating a recombination 'hotspot'. Recombination between strains EA and C was rare, despite their frequent co-infections in wild plants, suggesting purifying selection against strain EA/C recombinants. Positive selection was predicted on 17 amino acids distributed over the entire coat protein in the globally distributed strain C, as compared to only four amino acids in the coat protein N-terminus of the EA strain. This selection implies a more recent introduction of the C strain and a higher adaptation of the EA strain to the local ecosystem. Thus, East Africa appears as a hotspot for evolution and diversification of SPFMV.