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Speciation of two social parasites from their respective hosts is tested using a molecular phylogeny. Alignment of 711 DNA base pairs of mitochondrial cytochrome b gene was used to assess phylogenetic relationships of inquiline species to their hosts and to other members of the genus. We show that the inquiline social parasites of the North American seed harvester ants are monophyletic, descending from one of the known hosts (Pogonomyrmex barbatus) in the recent past and shifting hosts in a pattern similar to that observed in other Hymenopteran social parasites. In addition, the host populations unexpectedly were found to be polyphyletic. Populations of Pogonomyrmex rugosus from an area east of the Chiricahua Mountains in Southern Arizona belong to a mitochondrial clade separate from the more western clade of P. rugosus from the Sonoran and Chihuahuan Deserts. Evidence of mitochondrial DNA introgression between P. rugosits and P. barbatus was also observed. We conclude that Emery’s rule does not strictly hold for this system, but that the hosts and parasites are very closely related, supporting a loose definition of Emery’s rule.