We examined the effect of natural host-plant quality on immune resistance in the autumnal moth, Epirrita autumnata (Borkhausen) (Lepidoptera: Geometridae). The division of mountain birches [Betula pubescens ssp. czerepanovii (Orlova) Hämet-ahti (Betulaceae)] into two categories, high- and low-quality food for larvae, was based on previous years’ results on the relative growth rate of the autumnal moth on the trees selected. The strength of the immune defence of autumnal moths was determined by measuring their encapsulation rate to exposure to a foreign antigen and the phenoloxidase (PO) activity of the pupal haemolymph. We found that individuals reared as larvae on naturally low-quality food had a significantly higher encapsulation rate at the pupal stage than individuals reared on high-quality food. Females also had a higher encapsulation rate than males. Food quality did not have statistically significant effect on PO activity, nor did this response variable show any differences between the sexes. Using half-sib analyses, we found significant heritable variation in the encapsulation rate; the heritable variation in PO activity was near to significant, although equally strong. Heritability estimates (h2: 0.19–0.27) for immune defence traits were relatively low and only moderate when compared to other studies with insects. We also found a negative genetic correlation between pupal mass and PO activity, but not between PO activity and encapsulation rate. Our results suggest that the quality of food affects immune defence in the autumnal moth. Thus an intricate tritrophic relationship exists between the folivorous insect, the host tree, and the insect's natural enemies (e.g., pathogens, parasites, and parasitoids). This study demonstrates that natural variation within a food plant species has an effect on the innate immune system of an herbivorous insect.