Animal propulsors such as wings and fins bend during motion and these bending patterns are believed to contribute to the high efficiency of animal movements compared with those of man-made designs. However, efforts to implement flexible designs have been met with contradictory performance results. Consequently, there is no clear understanding of the role played by propulsor flexibility or, more fundamentally, how flexible propulsors should be designed for optimal performance. Here we demonstrate that during steady-state motion by a wide range of animals, from fruit flies to humpback whales, operating in either air or water, natural propulsors bend in similar ways within a highly predictable range of characteristic motions. By providing empirical design criteria derived from natural propulsors that have convergently arrived at a limited design space, these results provide a new framework from which to understand and design flexible propulsors.