Mating system plays a determinant role in the maintenance and distribution of genetic variation. Difficulties in applying standard methods of indirect inferences onto parasitic life-cycles partly explain the current lack of knowledge on parasite mating systems. The present study develops a combination of direct and indirect inference methods circumventing such difficulties, and illustrates in particular how such a combination modifies our understanding of the biology of the southern cattle tick, Rhipicephalus microplus. To directly assess how females and males pair in natural populations, we sampled 225 mating pairs, genotyped them at six microsatellite loci, and analysed the correlation between mating status and genetic relatedness. This analysis revealed pangamy, i.e. a random association of male and female genotypes. In addition, indirect methods inferred that sib-groups of ticks exploit distinct individual-cows, and hence that ticks probably move among cows during their parasitic lifetime. Altogether, these results negate the expectation of a high frequency of sib-mating, and show the coexistence of genetically diverging stocks within tick cohorts and populations. These results have several consequences for our understanding of R. microplus. For instance, while existing models of pesticide resistance management look perfectly applicable to this species, the epidemiological models of the micropathogens it vectors needs revision. More largely, the methods developed here would help clarify the evolutionary patterns of any dioceous parasite.