While most eukaryotes contain single regional centromeres, several plant and animal lineages assemble holocentromeres along the entire chromosome length. In our study, we assembled genomes of three beak sedges (Rhynchospora pubera
, R. breviuscula
, and R. tenuis
) with repeat-based holocentromeres as well as a genome of their closest monocentric relative, Juncus effusus
, and compared their genome organization and evolution as a function of centromere type. We demonstrate that transition to holocentricity influenced the 3D (epi)genome architecture by redefining genomic compartments, while distributing centromere function to thousands of repeat-based centromere units genome-wide. We also show that chromosome fusions, facilitated by repeat-based holocentromeres, promoted karyotype evolution and diploidization. The study thus shed light on several important aspects of genome architecture and evolution influenced by centromere organization.