We compared ancestral anadromous-marine and nonmigratory, stream-resident threespine stickleback (Gasterosteus aculeatus) populations to examine the outcome of relaxed selection on prolonged swimming performance. We reared marine and stream-resident fish from two locations in a common environment and found that both stream-resident populations had lower critical swimming speeds (Ucrits) than marine populations. F1 hybrids from the two locations displayed significant differences in dominance, suggesting that the genetic basis for variation in Ucrit differs between locations. To determine which traits evolved in conjunction with, and may underlie, differences in performance capacity we measured a suite of traits known to affect prolonged swimming performance in fish. Although some candidate traits did not evolve (standard metabolic rate and two body shape traits), multiple morphological (pectoral fin size, shape, and four body shape measures) and physiological (maximum metabolic rate; MMR) traits evolved in the predicted direction in both stream-resident populations. However, data from F1 hybrids suggested that only one of these traits (MMR) had dominance effects similar to those of Ucrit in both locations. Overall, our data suggest that reductions in prolonged swimming performance were selected for in nonmigratory populations of threespine stickleback, and that decreases in MMR may mediate these reductions in performance.