Blast, caused byMagnaporthe oryzae, is one of the most destructive diseases affecting rice production. Understanding population dynamics of the pathogen’s avirulence genes is pre-required for breeding and then deploying new cultivars carrying promising resistance genes. The divergence and population structure ofAvrPiiwas dissected in the populations of southern (Guangdong, Hunan, and Guizhou) and northern (Jilin, Liaoning, and Heilongjiang) China, via population genetic and evolutionary approaches. The evolutionary divergence between a known haplotypeAvrPii-J and a novel oneAvrPii-C was demonstrated by haplotype-specific amplicon-based sequencing and genetic transformation. The different avirulent performances of a set of seven haplotype-chimeric mutants suggested that the integrity of the full-length gene structures is crucial to express functionality of individual haplotypes. All the four combinations of phenotypes/genotypes were detected in the three southern populations, and only two in the northern three, suggesting that genic diversity in the southern region was higher than those in the northern one. The population structure of theAvrPiifamily was shaped by balancing, purifying, and positive selection pressures in the Chinese populations. TheAvrPii-J was recognized as the wild type that emerged before rice domestication. Considering higher frequencies of avirulent isolates were detected in Hunan, Guizhou, and Liaoning, the cognate resistance genePiicould be continuously used as a basic and critical resistance resource in such regions. The unique population structures of theAvrPiifamily found in China have significant implications for understanding how theAvrPiifamily has kept an artful balance and purity among its members (haplotypes) those keenly interact withPiiunder gene-for-gene relationships. The lesson learned from case studies on theAvrPiifamily is that much attention should be paid to haplotype divergence of target gene.