Genetic analysis of prairie and montane populations of Dermacentor andersoni (Stiles) originating from Alberta (AB) and British Columbia (BC), Canada, respectively, indicated limited gene flow (N_m < 1) and a large amount of genetic differentiation (F_st = 0.49) between the populations. The prairie population also had a greater level of genetic diversity. Mating experiments indicated that females of geographically heterogeneous crosses had similar engorgement and oviposition failure as homogenous crosses in the parental generation but that egg mass sterility was greatest for the AB♀ × BC♂ cross, intermediate for the homogenous crosses, and lowest for the BC♀ × AB♂ cross. The progeny of all crosses produced fertile eggs, and the only significant effect in the progeny generation was increased oviposition failure of the pure AB cross. Covariate analysis indicated that egg mass sterility was associated with BC males in the parental generation and that oviposition failure was associated with AB males and AB females in the progeny generation. The hazard of cumulative reproductive failure was increased with AB females in both generations, reduced for AB males in the parental generation, and increased with AB males in the progeny generation. Overall, heterogenous crosses had the greatest and least reproductive failure in the parental generation, but they were intermediate to the homogenous crosses in the progeny generation. The limited gene flow between the populations seems to have been sufficient to maintain reproductive compatibility.