The nucleolus is the most prominent nuclear organelle in almost all cells including mammalian oocytes and embryos. It is primarily responsible for ribosome biogenesis. However, non-canonical functions have been described and the list of potential nucleolar roles is expanding. Given that in oocytes ribosome-biogenesis and gene transcription shut down, non-canonical roles of the nucleolus are of particular interest in this cell type. In addition, the mature oocyte provides an ideal model in which to study these roles separable from ribosome biogenesis. However, the nucleolus is still relatively mysterious in these cells. Here we first discuss roles of the nucleolus in mitosis where they are relevant to the growing oocyte. We then focus on the role of the nucleolus as ribosome-biogenesis comes to a halt and transcription is silenced at the end of prophase I. Transcription remains silent in oocytes until activation of the embryonic genome, during which time oocytes and early embryos rely on a stockpile of maternal transcripts and proteins. Traditional literature suggested that the ‘silent’ nucleolus is not more than a passive dense mass, holding nucleolar proteins until they are again required to rebuild an organelle capable of ribosome biogenesis. However, the nucleolus now seems far from obsolete. Chromatin dispersed throughout the nucleoplasm undergoes remarkable rearrangements during the transitions between active-to-silenced and silenced-to-active transcription, appearing to use the nucleolus as a scaffold. Furthermore, a series of enucleolation experiments and other studies indicate the existence of a novel and essential role for the oocyte nucleolus following fertilisation. Importantly, a role that cannot be compensated for by a somatic cell nucleolus.