A key determinant of female reproductive lifespan is the size of the resting oocyte pool following extensive oocyte elimination during fetal and perinatal periods. Excessive oocyte culling occurs in response to excessive transposon activity, defects in meiotic prophase, and various forms of DNA damage. For example, in mice lacking SPO11 or MSH4, two key recombination factors, normal numbers of oocytes are present at birth, but most oocytes die within a few days. Rnf212 encodes a RING-family E3 ligase that promotes protein modification by the ubiquitin-like molecule, SUMO. We previously showed that RNF212 acts at recombination sites to promote chromosomal crossing over. Unexpectedly, we now show that Rnf212 mutation restores the resting oocyte pools of both Spo11 and Msh4 mutants. These data implicate RNF212-mediated SUMOylation as a novel aspect of the meiotic checkpoint-signaling pathway that leads to oocyte apoptosis.