Abstract When resources are limited, mean fitness is constrained and competition can cause genes and phenotypes to enhance an individual’s own fitness while reducing the fitness of their competitors. Negative social effects on fitness have the potential to constrain adaptation, but the interplay between ecological opportunity and social constraints on adaptation remains poorly studied in nature. Here, we tested for evidence of phenotypic social effects on annual fitness (survival and reproductive success) in a long-term study of wild North American red squirrels (Tamiasciurus hudsonicus) under conditions of both resource limitation and super-abundant food resources. When resources were limited, populations remained stable or declined, and there were strong negative social effects on annual survival and reproductive success. That is, mean fitness was constrained and individuals had lower fitness when other nearby individuals had higher fitness. In contrast, when food resources were super-abundant, populations grew and social constraints on reproductive success were greatly reduced or eliminated. Unlike reproductive success, social constraints on survival were not significantly reduced when food resources were super-abundant. These findings suggest resource-dependent social constraints on a component of fitness, which have important potential implications for evolution and adaptation.