Transmission ratio distortion (TRD) is frequently observed in inter- and intraspecific hybrids of plants, leading to a violation of Mendelian inheritance. Sex-independent TRD (siTRD) was detected in a hybrid between Asian cultivated rice and its wild ancestor. Here we examined how siTRD caused by an allelic interaction at a specific locus arose in Asian rice species. The siTRD is controlled by the S6 locus via a mechanism in which the S6 allele acts as a gamete eliminator, and both the male and female gametes possessing the opposite allele (S6a) are aborted only in heterozygotes (S6/S6a). Fine mapping revealed that the S6 locus is located near the centromere of chromosome 6. Testcross experiments using near-isogenic lines (NILs) carrying either the S6 or S6a alleles revealed that Asian rice strains frequently harbor an additional allele (S6n) the presence of which, in heterozygotic states (S6/S6n and S6a/S6n), does not result in siTRD. A prominent reduction in the nucleotide diversity of S6 or S6a carriers relative to that of S6n carriers was detected in the chromosomal region. These results suggest that the two incompatible alleles (S6 and S6a) arose independently from S6n and established genetically discontinuous relationships between limited constituents of the Asian rice population.