Obligate parthenogenesis is found in only 0.1% of vertebrate species, is thought to be relatively short lived and is typically of hybrid origin. However, neither the evolutionary persistence of asexuality in vertebrates, nor the conditions that allow the generation of new parthenogenetic lineages are currently well understood. It has been proposed that vertebrate parthenogenetic lineages arise from hybridisation between two divergent taxa within a specific range of phylogenetic distances (the “Balance Hypothesis”). Moreover, parthenogenetic species often maintain a certain level of hybridisation with their closest sexual relatives, potentially generating new polyploid hybrid lineages. Here we address the role of hybridisation in the origin and evolutionary lifespan of vertebrate parthenogens. We use a set of microsatellite markers to characterize the origins of parthenogens in the lizard genus Darevskia to study the distinctiveness of sexual and asexual taxa currently in sympatry, and to analyse the evolutionary consequences of interspecific hybridisation between asexual females and sexual males. We find that parthenogens result from multiple past hybridisation events between species from specific lineages over a range of phylogenetic distances. This suggests that the Balance Hypothesis needs to make allowance for lineage-specific effects, as envisaged in the “Phylogenetic Constraint Hypothesis”. Our results show recurrent backcrossing between sexual and parthenogenetic Darevskia but neither gene flow nor formation of new asexual lineages is found. We suggest that, along with their demographic advantage, parthenogens gain additional leverage to outcompete sexuals in nature when the retention of sexual reproductive machinery allows backcrossing with their sexual ancestors.