Determining how adaptive evolution can be coupled to ecological processes is key for developing a more integrative understanding of the demographic factors that regulate populations. Intraspecific competition is an especially important ecological process because it generates negative density dependence in demographic rates. Although ecological factors are most often investigated to determine the strength of density dependence, evolutionary processes such as local adaptation could also feed back to shape variation in the strength of density dependence among populations. Using an experimental approach with damselflies, a predaceous aquatic insect, we find evidence that both density-dependent intraspecific competition and local adaptation can reduce per capita growth rates. In some cases, the effects of local adaptation on reducing per capita growth rates exceeded the ecological competitive effects of a doubling of density. However, we also found that these ecological and evolutionary properties of populations are coupled, and we offer two interpretations of the causes underlying this pattern: (1) the strength of density-dependent competition depends on the extent of local adaptation, or (2) the extent of local adaptation is shaped by the strength of density-dependent competition. Regardless of the underlying causal pathway, these results show how eco-evolutionary dynamics can affect a key demographic process regulating populations.