Two distinct patterns of sequence diversity for the recessive alleles of two host factors HvPDIL5 - 1 and HvEIF4E indicated the adaptive selection for bymovirus resistance in cultivated barley from East Asia. Plant pathogens are constantly challenging plant fitness and driving resistance gene evolution in host species. Little is known about the evolution of sequence diversity in host recessive resistance genes that interact with plant viruses. Here, by combining previously published and newly generated targeted re-sequencing information, we systematically analyzed natural variation in a broad collection of wild (Hordeum spontaneum; Hs) and domesticated barleys (Hordeum vulgare; Hv) using the full-length coding sequence of the two host factor genes, HvPDIL5-1 and HvEIF4E, conferring recessive resistance to the agriculturally important Barley yellow mosaic virus (BaYMV) and Barley mild mosaic virus (BaMMV). Interestingly, two types of gene evolution conferred by sequence variation in domesticated barley, but not in wild barley were observed. Whereas resistance-conferring alleles of HvEIF4E exclusively contained non-synonymous amino acid substitutions (including in-frame sequence deletions and insertions), loss-of-function alleles were predominantly responsible for the HvPDIL5-1 conferred bymovirus resistance. A strong correlation between the geographic origin and the frequency of barley accessions carrying resistance-conferring alleles was evident for each of the two host factor genes, indicating adaptive selection for bymovirus resistance in cultivated barley from East Asia.