*Background and Aims Highly controlled experiments document that plant genetic diversity and relatedness can shape herbivore communities and patterns of herbivory. Evidence from the field is, however. scarce and inconsistent. We assessed whether a genetic signal underlying herbivory can be detected in oak woodlands when accounting for variation at smaller (within-tree) and larger (among-stand) scales. *Methods We tested relationships between tree genetic relatedness, leaf chemical defences and insect herbivory for different canopy layers in 240 trees from 15 pedunculate oak (Quercus robur) forest stands. We partitioned sources of variability in herbivory and defences among stands, individuals and branches. *Key Results Leaf defences, insect herbivory and their relationship differed systematically between the upper and the lower tree canopy. When accounting for this canopy effect, the variation explained by tree genetic relatedness rose from 2.8 to 34.1 % for herbivory and from 7.1 to 13.8 % for leaf defences. The effect was driven by markedly stronger relationships in the upper canopy. *Conclusions Our findings illustrate that considerable effects of the host plant genotype on levels of leaf chemical defences and associated insect herbivory can be detected in natural tree populations when within-individual variation is properly accounted for.