During oocyte maturation, fertilization, and early embryo development until zygotic genome activation (ZGA), transcription is suppressed, and gene expression is dependent upon the timely activation of stored mRNAs. Embryonic poly(A)-binding protein (EPAB) is the predominant poly(A)-binding protein in Xenopus, mouse, and human oocytes and early embryos and is important for regulating translational activation of maternally stored mRNAs. EPAB is critical for early development because Epab(-/-) female mice do not produce mature eggs and are infertile. In this study, we further characterize morphological and molecular aspects of Epab(-/-) oocytes. We demonstrated that Epab(-/-) oocytes are smaller in size, contain peripheral germinal vesicles, and are loosely associated with cumulus cells. The chromatin reorganization of the surrounded nucleolus (SN) configuration and transcriptional silencing that normally occurs during oocyte growth does not occur in Epab(-/-) oocytes. Interestingly, microinjection of Epab mRNA into Epab(-/-) preantral follicle-enclosed oocytes rescues reorganization of chromatin and oocyte maturation to metaphase II. Overall, these results demonstrate an important role for EPAB during oocyte growth and the acquisition of meiotic competence.