The course of wound healing, during all of its phases, involves the intricate coordination of both canonical and non-canonical signaling mechanisms that enable distinct cell populations in the skin to guide each other towards repair. Among the non-canonical signaling modalities, extracellular vesicles (EVs), which are constitutively released by nearly all cells, have surfaced as important mediators of this intercellular communication. By trafficking a host of signaling molecules, including nucleic acids, bioactive lipids, and proteins, EVs can influence the phenotype of neighboring cells upon uptake. In the context of cutaneous repair, stem cell-derived EVs have demonstrated therapeutic potential for treating chronic and non-healing wounds. While this underscores the regenerative capacity of exogenously administered EVs as a cell-free treatment, it is equally important to recognize the contribution of endogenously produced EVs in a native wound environment to the healing process. In fact, these vesicle-bound parcels of information are released by epithelial cells, immune cells, vascular cells, and matrix-depositing cells, linking their function to the complex network of signaling and communication that activates upon tissue injury. This review will synthesize the existing evidence on the function of skin cell- and stem cell-derived EVs in wound healing and tissue repair, and provide an outlook on the fundamental and translational approaches to studying EVs in skin regeneration.