A system traditionally known for DNA segregation has taken on a surprising new role in multicellular cyanobacteria. Instead of being involved in chromosome partitioning, we find that its disruption leads to dramatic changes in cell shape. Using a combination of live cell imaging, in vitro reconstitution, evolutionary and structural analyses, we identify a novel cytoskeletal system that interacts with the cell membrane and is spatially regulated by components of the division machinery. These findings highlight a surprising evolutionary shift from DNA segregation to cell shape determination, revealing unexpected repurposing in conserved protein systems.