Sex-determination mechanisms and sex chromosomes are known to vary among reptile species and, in a few celebrated examples, within populations of the same species. The oriental garden lizard, Calotes versicolor, is one of the most intriguing species in this regard, exhibiting evidence of multiple sex-determination modes within a single species. One possible explanation for this unusual distribution is that in C. versicolor, different modes of sex determination are confined to a particular population or a species within a cryptic species complex. Here, we report on a population genetic analysis using SNP data from a methylation-sensitive DArT sequencing analysis and mitochondrial DNA data obtained from samples collected from six locations: three from Bangladesh and three from Thailand. Our aim was to determine whether C. versicolor is best described as a single species with multiple lineages or as multiple species, as well as if its sex-determination mechanisms vary within or between species. We present evidence that the latter possibility is the case and that C. versicolor comprises a complex of cryptic species. We also identify sex-linked markers within these species and use them to identify modes of sex determination. Overall, our results suggest that different sex-determination modes have evolved among closely related species and within populations of Agamid lizards.