In contrast to their dioecious relatives, members of the parthenogenetic nematode genus Diploscapter harbor their entire genome within a single pair of highly heterozygous chromosomes. To examine how this unusual karyotype arose and how it may relate to the evolution of parthenogenesis, we generated chromosome-level assemblies for two species in this clade: Diploscapter pachys and Diploscapter coronatus. Sequence comparisons reveal that the two genomes are collinear across their entirety and that multiple ancestral chromosome fusions and extensive genomic rearrangements precede the divergence of these two species. The long sequencing reads capture the previously unidentified chromosome ends, capped by long subtelomeric repeat arrays and short telomere repeat arrays. Our analysis also identifies an introgression event after the divergence of these two species, suggesting that their parthenogenetic lifestyle may have been punctuated by rare sexual reproduction. These findings shed new light on how chromosome fusions, chromatin architecture, and reproductive strategies intersect in shaping chromosome evolution.