This project aimed to elucidate whether human follicular fluid–derived extracellular vesicles (ffEVs) enhance oocyte maturation during rescue in vitro maturation (rIVM). We characterised the protein cargo of ffEVs isolated from follicles containing oocytes at different maturation stages (GV, GVBD, and MII), identifying distinct proteomic signatures associated with follicular competence and oocyte maturity. Subsequently, single-cell proteomic profiling of IVM-matured oocytes supplemented with ffEVs demonstrated that ffEV treatment induces significant changes in oocyte protein abundance, including factors linked to oocyte maturation, endoplasmic reticulum function, steroid biosynthesis, and cytoskeletal organisation. These proteomic alterations were accompanied by changes in oocyte ultrastructure and organelle architecture.