A considerable number of earthworm species reproduce by parthenogenesis. This is the case for the cosmopolitan earthworm species, Aporrectodea trapezoides, although sexual forms have been described sporadically. We analyse 30 individuals from four localities where both forms appear in order to understand the evolutionary mechanisms related to parthenogenesis. Heterozygosity levels were higher in parthenogens, which may indicate a hybrid origin of parthenogenesis in this species. Significant genomic and microbiome differences were found only between the two reproductive types in Algerian earthworms. This could be explained by the fact that individuals from this population are obligate parthenogens, while those from Spain could be facultative parthenogens, erasing the traces that parthenogenesis might leave behind. Individuals have been found to be tetraploid. The fact of having an even ploidy makes possible the theory of two parthenogenesis types in this species. The differential loci between sexual and parthenogenetic individuals from Algeria were interestingly related to gametogenesis and symbiont-like processes. On the other hand, it seems that the microbiome has a phylogenetic component for more generic taxonomic ranges, while at the ZOTU level the soil in which they are found is more decisive. A total of 754 ZOTUs were differentially abundant between sexual and parthenogenetic Algerian earthworms, indicating the importance of the gut microbiome in the reproductive processes of this earthworm. These findings not only shed light on the complex interplay between genomic, microbiome, and reproductive mechanisms in A. trapezoides, but also present insights into the origin and persistence of parthenogenesis in earthworms.