Predators have a key role shaping competitor dynamics in food webs. Perhaps the most obvious way this occurs is when predators reduce competitor densities. However, consumption could also generate phenotypic selection on prey that determines the strength of competition, thus coupling consumptive and trait-based effects of predators. In a mesocosm experiment simulating fish predation on damselflies, we found that selection against high damselfly activity rates – a phenotype mediating predation and competition – weakened the strength of density-dependence in damselfly growth rates. A field experiment corroborated this finding and showed that increasing damselfly densities in lakes with high fish densities had limited effects on damselfly growth rates but generated a precipitous growth rate decline where fish densities were lower - a pattern expected because of spatial variation in selection imposed by predation. These results suggest that accounting for both consumption and selection is necessary to determine how predators regulate prey competitive interactions.