The planarian Schmidtea mediterranea can regenerate its entire body from small tissue fragments and is studied as whole-body regeneration model species. While well-annotated genome resources are critical for understanding regeneration, the assembly and functional analysis of planarian genomes has proven challenging due to extreme compositional biases (70% A/T), high repeat contents and limited utility of routine laboratory protocols owing to their divergent biochemistry. Only few and often fragmented genome assemblies are currently available, and open challenges include the provision of well-annotated chromosome-scale reference assemblies of the model species and other planarians for a comparative genome evolution perspective. Here we report a haplotype-phased, chromosome-scale genome assembly and high-quality gene annotations of the sexual strain of S. mediterranea. We also provide putative regulatory region annotations via optimized ATAC-seq and ChIP-seq protocols. To additionally leverage sequence conservation for regulatory element annotations, we generated annotated chromosome-scale genome assemblies and chromatin accessibility data for the three closest relatives of S. mediterranea: S. polychroa, S. nova, and S. lugubris. Although we find broad sequence divergence between the genomes, including in open chromatin regions, ChIP-mark bearing S. mediterranea regulatory elements displayed significant sequence conservation. The resulting high-confidence set of evolutionary conserved enhancers and promoters provides a valuable resource for the analysis of gene regulatory circuits and their evolution within the taxon. In addition, our four chromosome-scale genome assemblies provide a first comparative perspective on planarian genome evolution. Our analyses reveal frequent retrotransposon-associated chromosomal inversions and inter-chromosomal translocations that lead to a degradation of synteny across the genus. Interestingly, we further find independent and near-complete losses of the ancestral metazoan synteny across Schmidtea and two other flatworm groups, indicating that platyhelminth genomes largely evolve without syntenic constraints. We provide valuable genome resources for the planarian research community and set a foundation for comparative genomics of planarians. We find that the rapid structural evolution of planarian genomes contrasts with the conservation of regulatory elements. Therefore, the unusual biology of flatworms appears paired with equally unique patterns of genome evolution, in which the position of genes in the genome may not matter.