Centromeres are essential chromosomal regions responsible for ensuring proper chromosome segregation during cell division. Unlike monocentric chromosomes, which have a single centromeric region, holocentric chromosomes distribute centromeric activity along their entire length. This unique organization poses intriguing questions about its structure, function, and evolutionary origins. In this review, we outline recent advances in characterizing the molecular architectures of holocentric chromosomes in mitosis and meiosis, emphasizing both the shared features and lineage-specific adaptations that have evolved in plants and insects. A more detailed characterization of holocentric architectures across different lineages will also offer valuable insights into the potential mechanisms driving the evolutionary transition from monocentric to holocentric chromosomes.