Significance StatementCell division is one of the most fundamental processes of life at the cellular level. Here, we report a form of cell division that is driven by self-organized actin waves and, in contrast to conventional cytokinesis in animal cells, does not require the formation of an actomyosin contractile ring. Daughter cells that emerge from this process of wave-mediated cytofission have a well-controlled size and exhibit the so-called fan-shaped phenotype that is characterized by a stable elongated shape and highly persistent locomotion. In the framework of synthetic biology, this primitive form of cell division may serve as a paradigm of how to implement a self-organized proliferation strategy in artificial cells that are equipped with a minimal actin cortex.