In most eukaryotes cytokinesis is brought about by a contractile actin ring located at the division plane. Here, in fission yeast the actin ring was found to be required to generate late-mitotic microtubular structures located at the division plane, and these in turn maintained the medial position of the actin ring. When these microtubular structures were disrupted, the actin ring migrated away from the cell middle in a membrane traffic-dependent manner, resulting in asymmetrical cell divisions that led to genomic instability. We propose that these microtubular structures contribute to a checkpoint control that retains the equatorial position of the ring when progression through cytokinesis is delayed.