Although obligately asexual lineages are thought to experience selective disadvantages associated with reduced efficiency of fixing beneficial mutations and purging deleterious mutations, such lineages are phylogenetically and geographically widespread. However, despite several genome-wide association studies, little is known about the genetic elements underlying the origin of obligate asexuality and how they spread. Because most obligately asexual lineages have hybrid origins, it has been suggested that asexuality is caused by the unbalanced expression of alleles from the hybridizing species. Here, we investigate this idea by identifying genes with allele-specific expression (ASE) in a Daphnia pulex population, in which obligate parthenogens (OP) and cyclical parthenogens (CP) coexist, with the OP clones having been originally derived from hybridization between CP D. pulex and its sister species, D. pulicaria. OP D. pulex have significantly more ASE genes (ASEGs) than do CP D. pulex. Whole-genomic comparison of OP and CP clones revealed ~15,000 OP-specific markers and 42 consistent ASEGs enriched in marker-defined regions. Ten of the 42 ASEGs have alleles coding for different protein sequences, suggesting functional differences of the two parental alleles. Functional annotations of these ten genes suggest that at least three are directly involved in meiosis-related processes, e.g., RanBP2 can cause abnormal chromosome segregation in anaphase I, and the presence of Wee1 in immature oocytes leads to failure to enter meiosis II. These results provide a basis for future molecular resolution of the genetic basis of the transition to ameiotic parthenogenesis and the role of allele-specific expression.