Variance in edibility among plant genotypes is expected to be a key driver of plant genetic diversity (PGD) effects on abundance of insect herbivores and resulting herbivory. Yet, herbivore foraging behavior and leaf consumption may be also context-dependent and, in particular, influenced by herbivore density, which remains unexplored. We used a combination of field and laboratory experiments with saplings from four half-sib families (henceforth, families) of pedunculate oak (Quercus robur) to test how PGD and herbivore density interactively affect herbivory. Insect herbivory was assessed in a common garden experiment with plots containing all possible combinations of individuals from one to four oak families. Herbivore density was manipulated by spraying insecticide in a factorial design. Complementary feeding trials with gypsy moth larvae (Lymantria dispar) were used to further explore the mechanisms underlying observed patterns in the field. Herbivory decreased with increasing PGD under normal herbivore density, but not under reduced herbivore abundance. The most damaged oak family in the field was also the most consumed in non-choice tests and was consistently preferred over other families in choice tests. Trials showed that the presence of less edible families in the diet reduced overall consumption by gypsy moth larvae. Under field conditions, the most edible family consistently benefited most from being associated with less edible, neighboring genotypes. Our results demonstrate that small-scale PGD can provide associational resistance to insect herbivory, probably through change in herbivore foraging activity. Importantly, they also reveal that the magnitude of genetic diversity effect depends on herbivore density.