Two hundred years after Darwin's birth, our understanding of genetic mechanisms and cell biology has advanced to a level unimaginable in the 19th century. We now know that eukaryotic cells contain a huge variety of internal compartments, each with their own function, identity and history. For the compartments that together form the membrane-trafficking system, one of the central questions is how that identity is encoded and how it evolved. Here we review the key components involved in membrane-trafficking events, including SNAREs, Rabs, vesicle coats, and tethers and what is known about their evolutionary history. Our current understanding suggests a possible common mechanism by which the membrane-trafficking organelles might have evolved. This model of increased organellar complexity by gene duplication and co-evolution of multiple, interacting, specificity-encoding proteins could well be applicable to other non-endosymbiotic organelles as well. The application of basic evolutionary principles well beyond their original scope has been exceedingly powerful not only in reconstructing the history of cellular compartments, but for medical and applied research as well, and underlines the contributions of Darwin's ideas in modern biology.