Human folliculogenesis has been extensively reviewed, but gaps between morphology and molecular facets remain to be filled. We here detailed update human folliculogenesis at the morphological and molecular aspects and provided a link to oocyte maturation and competence acquisition, and, as well, to the novel findings on oocyte ultrastructure. While human folliculogenesis and oogenesis set the baseline of female fertility, a major challenge remains to bridge the gap between macro-morphological transitions and limited molecular pathways. Here, we provide a comprehensive review of recent conceptual advances in human follicular development, with a focus on emerging regulatory networks such as the Hippo and PI3K/mTOR pathways that regulate primordial follicle dormancy and activation. We combine classic morphological landmarks with recent quantitative stereological data to map the dynamic spatial reorganization of oocyte organelles (mitochondria, smooth endoplasmic reticulum complexes, and cortical vesicles) during prophase-I, metaphase-I and metaphase-II. Furthermore, we emphasize the translational significance of these cellular dynamics by connecting specific molecular checkpoints to clinical problems encountered in assisted reproduction. Understanding these synchronous nuclear-cytoplasmic maturation dynamics offers us important information to optimize in vitro maturation protocols, refine oocyte cryopreservation strategies and improve non-invasive quality assessments in reproductive medicine.