Asexual reproduction occurs widely in plants and animals, particularly in insects. Aphid species usually reproduce by cyclic parthenogenesis, but many species include obligate asexual lineages. We recently showed that the leaf-curl plum aphid, Brachycaudus helichrysi, actually encompasses two lineages, B. helichrysi H1 and H2. Ecological data suggest that these lineages have different life cycles. We conducted a large population genetics study, based on 14 microsatellite loci, to infer their respective life cycles and investigate their population structure and geographical distribution. Brachycaudus helichrysi H1 displayed the genetic signature of cyclical parthenogenesis, using plum trees as primary hosts for sexual reproduction, as classically described for B. helichrysi. This global survey showed that the Central Asian population of H1 was clearly differentiated from American–European populations. By contrast, B. helichrysi H2 displayed the typical signature of obligate asexual reproduction. H2 encompassed at least eight highly successful genotypes or superclones. This lack of ability to undergo sexual reproduction was confirmed for one of the superclones by sex induction experiments. We found only one B. helichrysi H2 population that underwent sexual reproduction, which was collected from peach trees, in Northern India. Our results confirm that H1 and H2 have different life cycles. Brachycaudus helichrysi H1 is clearly heteroecious using plum trees as primary hosts, while B. helichrysi H2 encompasses several anholocyclic lineages, and some heteroecious populations that until now have only been found associated with peach trees as primary hosts. We discuss implications of these findings for the pest status of B. helichrysi lineages.