Until recently, domestication has been interpreted as a rapid process with little predomestication cultivation and a relatively rapid rise of the domestication syndrome. This interpretation has had a profound effect on the biological framework within which investigations into crop origins have been carried out. A major underlying assumption has been that artificial selection pressures were substantially stronger than natural selection pressures, resulting in genetic patterns of diversity that reflect genetic independence of geographic localities. Recent archaeobotanical evidence has overturned the notion of a rapid transition, resulting in a protracted model that undermines these assumptions. Conclusions of genome-wide multilocus studies remain problematic in their support of a rapid-transition model by indicating that domesticated crops appear to be associated by monophyly with only a single geographic locality. Simulations presented here resolve this conflict, indicating that the results observed in such studies are inevitable over time at a rate that is largely influenced by the long-term population size. Counterintuitively, multiple origin crops are shown to be more likely to produce monophyletic clades than crops of a single origin. Under the protracted transition, the importance of the rise of the domestication syndrome becomes paramount in producing the patterns of genetic diversity from which crop origins may be deduced. We identify four different interacting levels of organization that now need to be considered to track crop origins from modern genetic diversity, making crop origins a problem that could be addressed through system-based approaches.