Prunus domestica commonly known as European plum is a hexaploid fruit tree species cultivated around the world. Locally it is used for fresh consumption, in jams or jellies, and the production of spirits while commercially the fruit is primarily sold dried (prunes). Despite its agricultural importance and long history of cultivation, many questions remain about the origin of this species, the relationships among its many pomological types, and its underlying genetics. Here, we used a sequence-based genotyping approach to characterize worldwide plum germplasm including the potential progenitor Eurasian plum species. Analysis of 405 DNA samples established a set of four clades consistent with the pomological groups Greengages, Mirabelles, European plums, and d’Agen (French) prune plums. A number of cultivars from each clade were identified as likely clonal selections, particularly among the “French” type prune germplasm that is widely cultivated today. Overall, there was relatively low genetic diversity across all cultivated plums suggesting they have been largely inbred and/or derived from a limited number of founders. The results agree with P. domestica having originated as an interspecific hybrid of a diploid P. cerasifera and a tetraploid P. spinosa that itself may have been an interspecific hybrid of P. cerasifera and an unknown Eurasian plum species. The low genetic diversity and lack of true wild-types coupled with the known cultivation history of Eurasian plums imply that P. domestica may have been a product of inter-specific cross breeding and artificial selection by early agrarian Eurasian societies.