Stem cell behavior, from rates of cell division to the capacity for self-renewal, is regulated by the specialized microenvironment in which those stem cells reside. A critical function of such niches in many tissues is the coordination of behavior across multiple stem cell lineages. However, the means by which this coordination is achieved are largely unknown. We have identified delayed completion of cytokinesis in germline stem cells (GSCs) as a novel mechanism that regulates the production of stem cell daughters within the testis niche. Through live imaging, we have characterized the delay within GSCs and identified two regulatory mechanisms layered on top of cytokinesis. Following contractile ring disassembly, a novel F-actin ring is formed exclusively in the stem cell population and only in male, but not female, GSCs. This ring is regulated by Cofilin activity and serves to block cytokinesis progress. The duration of this block is controlled by Aurora B activity. Additionally, we have identified a critical requirement for somatic cell encystment of the germline in promoting the final step of GSC cytokinesis. We suggest that this non-autonomous role exists to promote the coordination necessary between stem cell lineages within this niche to achieve robust production of sperm. Together, these findings shed significant insight into a niche-imposed block and reinitiation of cytokinesis in GSCs and why such complex regulation might exist within a stem cell niche.