Female meiosis involves two successive divisions driven by the activities of two major kinases, Cdk1 and MAPK. To date, the role of MAPK in control of meiosis is thought to be restricted to maintaining metaphase II arrest through stabilizing Cdk1 activity. Our study reports novel roles for MAPK in contributing to meiotic control. We find that MAPK and Cdk1 play compensatory roles to suppress APC activity early in prometaphase, thereby allowing accumulation of APC substrates essential for meiosis I. Furthermore, inhibition of MAPK at the onset of APC activity at the transition from meiosis I to meiosis II leads to accelerated completion of meiosis I and an increase in aneuploidy at metaphase II. These effects appear to be mediated via a Cdk1/MAPK-dependent stabilization of the spindle assembly checkpoint that when inhibited leads to increased APC activity. These findings suggest new roles for MAPK in regulation of meiosis in mammalian oocytes.