How did the vesicle traffic system of primordial eukaryotes expand to its present sophisticated form? Distinct paralogous copies of genes that regulate vesicle budding and fusion act at distinct subcellular locations, suggesting a link between the expansion of vesicle traffic pathways and the duplication of genes. We find that interspecies hybridization is a potent source of such duplications. We trace the history of paralog doublets derived from the 100-million-year-old hybridization event that gave rise to the whole genome duplication clade of budding yeast. We find that doublets encoding specific functional classes of vesicle traffic modules are convergently retained across species, leading to an expansion of the secretory apparatus across the entire clade. Our results show how a single hybridization event can have a long-term impact on cellular evolution. They suggest that common selective pressures for increased secretion have sculpted vesicle traffic pathways across diverse yeast species.