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The enigma of why sexual reproduction persists in nature despite its many costs continues to challenge the field of evolutionary biology. Compared to sexual reproduction, asexuality is more straightforward. However, it is rare in animals and often regarded as an evolutionary dead-end. ‘Ancient asexuals’ challenge this view, as they successfully persisted over evolutionary time. Understanding how these evolutionary scandals thrive in the absence of sex will, in turn, provide insights into the selective advantage of sexual reproduction. This thesis explored the consequences of ancient asexuality and emphasized its effects on genome evolution in natural populations. The oribatid mite Platynothrus peltifer was introduced as an ideal subject for studying ancient asexuality and speciation. Employing a comprehensive approach, I generated genome, transcriptome, and population data. Within this data, we found evidence of intra-individual haplotype divergence, conserved genomic synteny among populations, and notable inter-individual population variation. Thus, we proposed haplotypic independence to contribute to evolvability as a way to adapt and escape extinction in long-term asexuals. P. peltifer is known to exhibit multiple independent evolutionary lineages. Asexual speciation may be more prevalent in certain taxa, like oribatid mites, due to their distinctive ecological niches and long-term evolutionary persistence. Understanding how asexuals diversify into new species is crucial as it challenges traditional evolutionary paradigms, reveals hidden biodiversity, and provides insights into the dynamics of speciation, evolution, taxonomy, and conservation. Thus, this study delved into the complexities of species delimitation, while emphasizing the need for a holistic perspective in comprehending asexual speciation. I suggested speciation of the Japanese population and identified potential cryptic lineages in the Canadian population of P. peltifer. European populations lacked