Asexual reproduction is usually considered as an evolutionary dead end, and difficulties for asexual lineages to adapt to a fluctuating environment are anticipated due to the lack of sufficient genetic plasticity. Yet, unlike their sexual congeners, mitotic parthenogenetic root-knot nematode species, Meloidogyne spp., are remarkably widespread and polyphagous, with the ability to parasitize most flowering plants. Although this may reflect in part the short-term stability of agricultural environments, the extreme parasitic success of these clonal species points them as an outstanding evolutionary paradox regarding current theories on the benefits of sex. The discovery that most of the genome of the clonal species M. incognita is composed of pairs of homologous but divergent segments that have presumably been evolving independently in the absence of sexual recombination has shed new light on this evolutionary paradox. Together with recent studies on other biological systems, including the closely related sexual species M. hapla and the ancient asexual bdelloid rotifers, this observation suggests that functional innovation could emerge from such a peculiar genome architecture, which may in turn account for the extreme adaptive capacities of these asexual parasites. Additionally, the higher proportion of transposable elements in M. incognita compared to M. hapla and other nematodes may also be responsible in part for genome plasticity in the absence of sexual reproduction. We foresee that ongoing sequencing efforts should lead soon to a genomic framework involving genetically diverse Meloidogyne species with various different reproductive modes. This will undoubtedly promote the entire genus as a unique and valuable model system to help deciphering the evolution of asexual reproduction in eukaryotes.