The race-specific resistance gene Pi-ta has been effectively used to control blast disease, one of the most destructive plant diseases worldwide. A single amino acid change at the 918 position of the Pi-ta protein was known to determine resistance specificity. To understand the evolutionary dynamics present, we examined sequences of the Pi-ta locus and its flanking regions in 159 accessions composed of seven AA genome Oryza species: O. sativa, O. rufipogon, O. nivara, O. meridionalis, O. glaberrima, O. barthii, and O. glumaepatula. A 3364-bp fragment encoding a predicted transposon was found in the proximity of the Pi-ta promoter region associated with the resistance phenotype. Haplotype network analysis with 33 newly identified Pi-ta haplotypes and 18 newly identified Pi-ta protein variants demonstrated the evolutionary relationships of Pi-ta haplotypes between O. sativa and O. rufipogon. In O. rufipogon, the recent directional selection was found in the Pi-ta region, while significant deviation from neutral evolution was not found in all O. sativa groups. Results of sequence variation in flanking regions around Pi-ta in O. sativa suggest that the size of the resistant Pi-ta introgressed block was at least 5.4 Mb in all elite resistant cultivars but not in the cultivars without Pi-ta. These findings demonstrate that the Pi-ta region with transposon and additional plant modifiers has evolved under an extensive selection pressure during crop breeding.