Extracellular vesicles (EVs) are now understood to be ubiquitous mediators of cellular communication. In this review, we suggest that EVs have evolved into a highly regulated system of communication with complex functions including export of wastes, toxins and nutrients, targeted delivery of immune effectors, and vectors of RNA silencing. Eukaryotic EVs come in different shapes and sizes and have been classified according to their biogenesis and size distributions. Small EVs (sEVs or exosomes) are released through fusion of endosome-derived multivesicular bodies (MVBs) with the plasma membrane. Medium EVs (mEVs or microvesicles) bud off the plasma membrane as a form of exocytosis. Finally, large EVs (lEVs or apoptotic bodies) are produced as a result of the apoptotic process. This review considers EV secretion and uptake in four eukaryotic kingdoms, three of which produce cell walls. The impact cell walls have on EVs in plants and fungi are discussed, as are roles of fungal EVs in virulence. Contributions of plant EVs to development and innate immunity are presented. Compelling cases are sporophytic self-incompatibility and cellular invasion by haustorium-forming filamentous pathogens. The involvement of EVs in all of these eukaryotic processes is reconciled considering their evolutionary history.