During male and female gametogenesis in species ranging from insects to mammals, germ cell cyst formation by incomplete cytokinesis involves the stabilization of cleavage furrows and the formation of stable intercellular bridges called ring canals. Accurate regulation of incomplete cytokinesis is required for both female and male fertility in Drosophila melanogaster. Nevertheless, the molecular mechanisms controlling complete versus incomplete cytokinesis are largely unknown. Here, we show that the scaffold protein Cindr is a novel component of both mitotic and meiotic ring canals during Drosophila spermatogenesis. Strikingly, unlike other male germline ring canal components, including Anillin and Pavarotti, Cindr and contractile ring F-actin dissociate from mitotic ring canals and translocate to the fusome upon completion of the mitotic germ cell divisions. We provide evidence that the loss of Cindr from mitotic ring canals is coordinated by signals that mediate the transition from germ cell mitosis to differentiation. Interestingly, Cindr loss from ring canals coincides with completion of the mitotic germ cell divisions in both Drosophila females and males, thus marking a common step of gametogenesis. We also show that Cindr co-localizes with Anillin at mitotic and meiotic ring canals and is recruited to the contractile ring by Anillin during male germ cell meiotic cytokinesis. Taken together, our analyses reveal a key step of incomplete cytokinesis at the endpoint of the mitotic germ cell divisions in D. melanogaster.