The widespread occurrence of sex is one of the most elusive problems in evolutionary biology. Theory predicts that asexual lineages can be driven to extinction by uncontrolled proliferation of vertically transmitted transposable elements (TEs), which accumulate because of the inefficiency of purifying selection in the absence of sex and recombination. To test this prediction, we compared genome-wide TE load between a sexual lineage of the parasitoid wasp Leptopilina clavipes and a lineage of the same species that is rendered asexual by Wolbachia-induced parthenogenesis. We obtained draft genome sequences at 15–20× coverage of both the sexual and the asexual lineages using next-generation sequencing. We identified transposons of most major classes in both lineages. Quantification of TE abundance using coverage depth showed that copy numbers in the asexual lineage exceeded those in the sexual lineage for DNA transposons, but not LTR and LINE-like elements. However, one or a small number of gypsy-like LTR elements exhibited a fourfold higher coverage in the asexual lineage. Quantitative PCR showed that high loads of this gypsy-like TE were characteristic for 11 genetically distinct asexual wasp lineages when compared to sexual lineages. We found no evidence for an overall increase in copy number for all TE types in asexuals as predicted by theory. Instead, we suggest that the expansions of specific TEs are best explained as side effects of (epi)genetic manipulations of the host genome by Wolbachia. Asexuality is achieved in a myriad of ways in nature, many of which could similarly result in TE proliferation.