Sporulation is a unique form of cytokinesis that occurs following meiosis II in many yeasts, during which four daughter cells (spores) are generated within a single mother cell. Here we characterize the role of F-actin in the process of sporulation in the fission yeast Schizosaccharomyces pombe. As shown previously, we find that F-actin assembles into four ring structures per ascus, referred to as the meiotic actin ring (MeiAR). The actin nucleators Arp2/3 and formin For3 assemble into ring structures that overlap with Meu14, a protein known to assemble into the so-called leading edge, a ring structure that is known to guide forespore membrane assembly. Interestingly, F-actin makes rings that occupy a larger region behind the leading edge ring. Time-lapse microscopy showed that the MeiAR assembles near the spindle pole bodies and undergoes an expansion in diameter during the early stages of meiosis II, followed by closure in later stages of meiosis II. MeiAR closure completes the process of forespore membrane assembly. Loss of the MeiAR leads to excessive assembly of forespore membranes with a deformed appearance. The rate of closure of the MeiAR is dictated by the function of the septation initiation network (SIN). We conclude that the MeiAR ensures proper targeting of the membrane biogenesis machinery to the leading edge, thereby ensuring the formation of spherical spores.