Oogenesis requires complex interactions amongst germline and somatic cell types in the ovary. How did these cell types and their signaling interactions evolve? Here we use the sea star Patiria miniata as a non-chordate deuterostome representative to define the ovarian cell type toolkit in echinoderms. Sea stars continuously produce millions of new oocytes throughout their lifespan, making them a practical system to understand the mechanisms that drive oogenesis from a biomedical and evolutionary perspective. We performed scRNA-seq combined with high-resolution 3D-imaging to reveal the ovarian cell types and their spatial organization. Our data support the presence of actively dividing putative oogonial stem cells and granulosa-like and theca-like cells, which display similarities and possible homology with their mammalian counterparts. Lastly, our data may suggest the existence of an intrinsic neuroendocrine system which could potentially control oogenesis and predates the formation of the hypothalamic-pituitary-gonadal axis in vertebrates.