The Mos kinase is exclusively expressed in oocytes and is degraded upon fertilization. When present, Mos constitutively activates the ERK/MAPK pathway. This atypical activation of ERK/MAPK during meiotic divisions has been documented across animal phyla, from the non-bilaterian cnidarians to mammals. However, the inherent diversity of reproductive strategies and the consequent variability in timing and morphology of meiotic divisions complicates the identification of conserved molecular mechanisms under the control of Mos-MAPK. In this review, we synthesize data from different species in an attempt to identify conserved downstream functional modules. We first provide an overview of the cellular functions necessary for execution of the specialized meiotic divisions of oocytes, and detail those that have been found to be under the control of Mos-MAPK. We then discuss how Mos-MAPK may be a universal regulator of the meiotic cell cycle by controlling translation of cyclin B and other factors. Secondly, we discuss how ensuring the asymmetry of meiotic divisions may be another conserved function regulated by Mos-MAPK acting on the microtubule spindle and on the cytokinetic machinery.