Extracellular vesicles (EVs) mediate ocular immune communication, and their biological effects depend heavily on their cell of origin, activation state, recipient tissue, and route of exposure. This narrative review examines endogenous EV signaling and therapeutic EV preparations across the ocular surface, cornea, uvea, retina, and optic nerve, distinguishing mechanistic evidence from biomarker associations and treatment outcomes. Endogenous EVs can transfer alloantigens, recruit leukocytes, and amplify glial and vascular inflammation. Conversely, EVs from selected stromal and regulatory immune cells suppress inflammation in experimental models of dry eye, keratitis, uveitis, and neuroretinal injury. Reported protective mechanisms include modulation of antigen presentation, T helper 17/regulatory T cell balance, inflammasome activity, and microglial–neurovascular interactions. These mechanisms vary among models and are not established across all ocular compartments. Small dry-eye trials support further clinical investigation, while negative results, model dependence, and limited durability constrain broader claims of efficacy. A source–state–recipient–exposure framework helps explain divergent findings and identifies translation priorities: reproducible product characterization, appropriate non-vesicular controls, mechanism-informed potency assays, and indication-specific delivery. Establishing whether endogenous EVs are required for ocular immune homeostasis, and whether administered preparations produce sustained clinical benefit without compromising host defense, remains central to the field.