The early developmental events of all multicellular animals are governed by the maternal genome. Maternal RNA plays a crucial role in sustaining the viability and growth of the early embryo, providing molecular instructions for each initial cell division and facilitating the transition to embryonic development under zygotic genome control. Consequently, the fate of each blastomere depends on its set of maternal determinants, which may be critically important for the successful progression of stereotypical and invariant cleavage patterns observed in spiralian animals. How is maternal RNA distributed in the embryo of a typical spiralian animal? What is its quantity, and for how long is it preserved? The laboratory annelid, P. dumerilii, serves as an excellent model to address these questions. We quantified the average amount of maternal RNA in a single oocyte of this species and examined its localization in oocytes and early embryos, prior to zygotic genome activation. Our findings reveal that maternal RNA in P. dumerilii is initially distributed around the oocyte nucleus and rapidly relocates to the animal pole following fertilization. Its subsequent segregation closely aligns with unequal-cleavage dynamics. One cell cycle prior to the first wave of zygotic transcription, nearly all maternal RNA becomes concentrated in the first quartet of micromeres 1a1-1d1 and the first somatoblast 2d. The descendants of 2d undergo bilateral division, ultimately giving rise to all ectodermal derivatives in both the larva and the adult worm. These findings raise important questions regarding the relative contributions of maternal and zygotic factors during the bilateral phase of cleavage in annelids. Our study highlights P. dumerilii as a compelling and valuable model for exploring the transition of early developmental control from the maternal to the zygotic genome.