Medusae were the earliest animals to evolve muscle-powered swimming in the seas. Although medusae have achieved diverse and prominent ecological roles throughout the world’s oceans, we argue that the primitive organization of cnidarian muscle tissue limits force production and, hence, the mechanical alternatives for swimming bell function. We use a recently developed model comparing the potential force production with the hydrodynamic requirements of jet propulsion, and conclude that jet production is possible only at relatively small bell diameters. In contrast, production of a more complex wake via what we term rowing propulsion permits much larger sizes but requires a different suite of morphological features. Analysis of morphometric data from all medusan taxa independently confirms size-dependent patterns or bell forms that correspond with model predictions. Further, morphospace analysis indicates that various lineages within the Medusozoa have proceeded along either of two evolutionary trajectories. The first alternative involved restriction of jet-propelled medusan bell diameters to small dimensions. These medusae may be either solitary individuals (characteristic of Anthomedusae and Trachymedusae) or aggregates of small individual medusan units into larger colonial forms (characteristic of the nectophores of many members of the Siphonophorae). The second trajectory involved use of rowing propulsion (characteristic of Scyphozoa and some hydromedusan lineages such as the Leptomedusae and Narcoinedusae) that allows much larger bell sizes. Convergence on either of the differing propulsive alternatives within the Medusozoa has emerged via parallel evolution among different medusan lineages. The distinctions between propulsive modes have important ecological ramifications because swimming and foraging are interdependent activities for medusae. Rowing swimmers are characteristically cruising predators that select different prey types from those selected by jet-propelled medusae, which are predominantly ambush predators. These relationships indicate that the different biomechanical solutions to constraints on bell function have entailed ecological consequences that are evident in the prey selection patterns and trophic impacts of contemporary medusan lineages.