Trait variation is central to our understanding of species interactions, and trait variation arising within species is increasingly recognized as an important component of community ecology. Ecologists generally consider intraspecific variation either among or within populations, yet these differences can interact to create patterns of species interactions. These differences can also affect species interactions by altering processes occurring at distinct scales. Specifically, intraspecific variation may shape species interactions simply by shifting a population’s position along a trait-function map, or by shifting the relationship between traits and their ecological function. I test these ideas by manipulating within- and among-population intraspecific variation in wild populations of a gall-forming insect, before quantifying species interactions and phenotypic selection. Within- and among-population differences in gall size interact to affect attack rates by an enemy community, but among-population differences were far more consequential. Intraspecific differences shaped species interactions both by shifting the position of populations along the trait-function map, and by altering the relationship between traits and their function, with ultimate consequences for patterns of natural selection. I suggest that intraspecific variation can affect communities and natural selection by acting through individual- and population-level mechanisms.