The bulb onion (Allium cepa L.) was historically seed propagated by open pollination (OP). Cytoplasmic-genic male sterility (CMS) and protandry encourage outcrossing among individual onion plants. The most common source of CMS in onion is conditioned by the interaction of sterile (S) cytoplasm with a single nuclear male-fertility restoration (Ms) locus. We previously reported that the majority of OP onion populations possess normal (N) male-fertile cytoplasm and varying frequencies of the dominant Ms allele. It was unclear why N-cytoplasmic onion populations often possess relatively high frequencies of the Ms allele, which has no obvious function. We used computer simulations to estimate changes in allelic frequencies at Ms for onion populations possessing S-cytoplasm or a mixture of N- and S-cytoplasms, and to determine if frequencies of the Ms allele stay constant or change due to failure of male gamete production from male-sterile (S msms) plants. The models revealed selection against the recessive ms allele over generations in onion populations possessing S-cytoplasm and varying amounts of self pollination and inbreeding depression. These models were consistent with field and molecular analyses documenting that N- cytoplasm and the dominant Ms allele predominate in OP onion populations.