Oocyte hydration is a critical physiological event determining egg quality and reproductive success in marine teleosts that produce pelagic eggs; however, the functional contribution of the surrounding follicular layer remains largely unexplored. In this study, we used the orange-spotted grouper (Epinephelus coioides) as a model to systematically characterize the transcriptional dynamics of the follicular layer during oocyte maturation. Integrated mRNA-seq and miRNA-seq analyses demonstrated a pronounced biphasic transcriptional regulatory pattern in the follicular layer during oocyte maturation. Early maturation was characterized by suppression of basal translational machinery and enhancement of mitochondrial oxidative phosphorylation, whereas late maturation was marked by the activation of cell cycle regulation and structural remodeling pathways. By constructing a multi-layered miRNA-transcription factor (TF)-mRNA regulatory network, we identified several key hub genes, including HSD17B1, VIPR1, and IGFBP2, which are involved in steroidogenic transitions and local signaling regulation. Notably, dual-luciferase reporter assays confirmed that novel-miR-88 and miR-338-3p directly target and repress AQP1a, revealing a crucial miRNA-mediated "braking" mechanism that maintains follicular structural stability. Collectively, this study provides valuable molecular targets for improving artificial reproduction and egg quality in marine aquaculture species.