The Arf family GTPases are regulators of eukaryotic cellular organization, with functions in processes such as vesicle budding, membrane tethering, microtubule dynamics, actin cytoskeleton regulation and lipid dynamics. We describe the evolution of this protein family and its well-studied regulators. The last eukaryotic common ancestor had fifteen members, and the current complement of Arf GTPases has been sculpted by gene loss and gene duplications since that point. Some Arf family GTPases (such as those which recruit vesicle coats in the secretory pathway) are present in virtually all eukaryotes, whereas others (such as those functioning in cilia and flagella) have a more limited distribution. A challenge for the future is understanding the full spectrum of Arf family functions throughout eukaryotes.