Strategies to position the division apparatus exhibit a bewildering diversity [1], but how these mechanisms evolve remains virtually unknown. Here, we explore the plasticity of division site positioning in fission yeasts Schizosaccharomyces pombe and Schizosaccharomyces japonicus. We demonstrate that, whereas both species divide in the middle, only S. pombe uses the anillin Mid1 as a primary nucleus-derived cue to assemble the actomyosin ring at the equatorial cortex. We trace this variance to the divergence in subcellular targeting of Mid1 and show that duplication of an ancestral anillin early in the Schizosaccharomyces lineage may have led to subfunctionalization of the Mid1 orthologs. In contrast to S. pombe, medial assembly of the actomyosin ring in mitotic S. japonicus relies on the cortical anchor protein Cdc15 regulated by the tip-localized kinase Pom1. Our data suggest that division site placement is determined by cortical positioning of the actomyosin-plasma membrane linkers and that both identity of the linker and control of its subcellular targeting are highly modular.