Cumulus cells and mural granulosa cells (MGCs) are spatially and functionally distinct cell types in antral follicles: cumulus cells contact the oocyte and most MGCs contact the basal lamina. For transcriptomic analyses, both cell types were collected from small and large antral follicles, before and after stimulation of immature mice with eCG, respectively. Both cell types underwent dramatic transcriptomic changes and the differences between them became greater with follicular growth. Although cumulus cells of both stages of follicular development are competent to undergo expansion in vitro, they were otherwise remarkably dissimilar with transcriptomic changes quantitatively equivalent to those of MGCs. Gene Ontology (GO) analysis showed that cumulus cells of small follicles were enriched in transcripts generally associated with catalytic components of metabolic processes while those from large follicles were involved in regulation of metabolism, cell differentiation, and adhesion. Upon contrasting cumulus cells versus MGCs, cumulus cells were enriched in transcripts associated with metabolism and cell proliferation while MGCs were enriched for transcripts involved in cell signaling and differentiation.