Aggressive behaviours are necessarily expressed in a social context, such that individuals may be influenced by the phenotypes, and potentially the genotypes, of their social partners. Consequently, it has been hypothesized that indirect genetic effects (IGEs) arising from the social environment will provide a major source of heritable variation on which selection can act. However, there has been little empirical scrutiny of this to date. Here we test this hypothesis in an experimental population of deer mice (Peromyscus maniculatus). Using quantitative genetic models of five aggression traits, we find repeatable and heritable differences in agonistic behaviours of focal individuals when presented with an opponent mouse. For three of the traits, there is also support for the presence of IGEs, and estimated correlations between direct and indirect genetic (rAO,F) effects were high. As a consequence, any selection for aggression in the focal individuals should cause evolution of the social environment as a correlated response. In two traits, strong positive rAO,F will cause the rapid evolution of aggression, while in a third case changes in the phenotypic mean will be constrained by negative covariance between direct and IGEs. Our results illustrate how classical analyses may miss important components of heritable variation, and show that a full understanding of evolutionary dynamics requires explicit consideration of the genetic component of the social environment.