Gymnosomatous pteropods are highly specialized planktonic predators that feed exclusively on their thecosomatous relatives. Feeding behavior and the morphology of gymnosome feeding structures are diverse and have evolved in concert with the size, shape, and consistency of the thecosome shell. Here, we show that the metabolic capacity and locomotory behaviors of gymnosomes are similarly diverse and vary with those of their prey. Both gymnosomes and thecosomes range from gelatinous sit-and-wait forms to active predators with high-performance locomotory muscles. We find more than 10-fold variation in size-adjusted and temperature-adjusted metabolic rates within both the Gymnosomata and Thecosomata and a strong correlation between the metabolic rates of predators and of prey. Furthermore, these characteristics are strongly influenced by environmental parameters and predator and prey converge upon similar physiological capacities under similar selection. For example, compensation of locomotory capacity in cold waters leads to elevated metabolic rates in polar species. This highly coevolved system is discussed in terms of a predator–prey “arms race” and the impending loss of both predator and prey as elevated atmospheric carbon dioxide levels threaten to dissolve prey shells via oceanic acidification.