The subgenus Crematogaster (Oxygyne) shows an Old World distribution and comprises a group of ants with specialised queen morphology suggestive of temporary social parasitism. This study investigated species hypotheses for Oxygyne species in Madagascar by integrating morphology and mitochondrial and nuclear sequences in an iterative taxonomic approach. Phylogenetic analyses (mrbayes and raxml) of one mitochondrial gene (cytochrome oxidase I) and analysis of population genetic structure (structure) based on three nuclear markers (long wavelength rhodopsin, arginine kinase, carbomoyl phosphate synthase) yielded a contrast between complex morphological variation and genetic data in six previously described species and subspecies. Thus, the taxonomy of the Malagasy Oxygyne is revised and three species are recognised: Crematogaster ranavalonae Forel, C. agnetis Forel and C. marthae Forel. The previously described C. ranavalonae pepo Forel, C. ranavalonae paulinae Forel, C. emmae Forel, C. emmae laticeps Forel, C. inops Forel and C. descarpentriesi Santschi are synonymised under C. ranavalonae, a species that is morphologically highly variable and shows exceptional polymorphism in the queen caste. Species descriptions and identification keys based on worker and queen ants are provided. A taxonomic synopsis, updated species list and morphological diagnosis of the entire subgenus Oxygyne is presented, and the subgenus Nematocrema is hereby synonymised under Oxygyne. Phylogenetic estimations (mrbayes, raxml, *beast) explore relationships between Malagasy and four other African and Asian taxa within Oxygyne and are based on both mitochondrial DNA and nuclear DNA sequences. The monophyly of the subgenus Oxygyne is strongly supported and the Malagasy Oxygyne form a clade that is sister to a clade of both African and an Asian taxa. Social parasitism is discussed as the cause for complex morphological variation in queens of C. ranavalonae, and phylogenetic results lead to the hypothesis of a single origin of this highly specialised queen caste in Crematogaster in the Old World. These findings highlight the need for field studies to explore the temporary parasitic behaviour and host–parasite relationships in these enigmatic ants, and to increase phylogenetic sampling to further investigate the evolution of this intriguing trait.