Cytoplasmic male sterility (CMS) is a widely used genetic tool in modern hybrid rice breeding. Most genes conferring rice gametophytic CMS are homologous to orf79 and co-transcribe with atp6. However, the origin, differentiation and flow of these mitochondrial genes in wild and cultivated rice species remain unclear. In this study, we performed de novo assembly of the mitochondrial genomes of 221 common wild rice (Oryza rufipogon Griff.) and 369 Asian cultivated rice (Oryza sativa L.) accessions, and identified 16 haplotypes of atp6-orf79-like structures and 11 orf79 alleles. These homologous structures were classified into 4 distinct groups (AO-I, AO-II, AO-III and AO-IV), all of which were observed in O. rufipogon but only AO-I was detected in O. sativa, causing a decrease in the frequency of atp6-orf79-like structures from 19.9% to 8.1%. Phylogenetic and biogeographic analyses revealed that the different groups of these gametophytic CMS-related genes in O. rufipogon evolved in a multicentric pattern. The geographical origin of the atp6-orf79-like structures was further traced back, and a candidate region in north-east of Gangetic Plain on the Indian Peninsula (South Asia) was identified as the origin centre of AO-I. The orf79 alleles were detected in all three cytoplasmic types (Or-CT0, Or-CT1 and Or-CT2) of O. rufipogon, but only two alleles (orf79a and orf79b) were observed in Or-CT0 type of O. sativa, while no orf79 allele was found in other types of O. sativa. Our results also revealed that the orf79 alleles in cultivated rice originated from the wild rice population in South and South-East Asia. In addition, strong positive selection pressure was detected on the sequence variations of orf79 alleles, and a special evolutionary strategy was noted in these gametophytic CMS-related genes, suggesting that their divergence could be beneficial to their survival in evolution.