Genes involved in plant defences against herbivores and pathogens are often highly polymorphic. This is a putative sign that balancing selection may have operated reciprocally on the hosts and their herbivores. Spatial and temporal variations (for example, in soil nutrients and the plants' ontogenetic development) may also modulate resistance traits, and thus selection pressures, but have been largely overlooked in theories of plant defences. Important elements of defences in
Populus tremula
(hereafter aspen) are phenolic compounds, including condensed tannins (CTs). Concentrations of CTs vary considerably with both variations in external factors and time, but they are also believed to provide genotype‐dependent resistance, mainly against chewing herbivores and pathogens. However, evidence of their contributions to resistance is sparse. Detailed studies of co‐evolved plant–herbivore associations could provide valuable insights into these contributions. Therefore, we examined correlations between CT levels in aspen leaves and both the feeding behavior and reproduction of the specialist aspen leaf aphid (
Chaitophorus tremulae
) in varied conditions. We found that xylem sap intake and probing difficulties were higher on genotypes with high‐CT concentrations. However, aphids engaged in more nonprobing activities on low‐CT genotypes, indicating that CTs were not the only defence traits involved. Thus, high‐CT genotypes were not necessarily more resistant than low‐CT genotypes, but aphid reproduction was generally negatively correlated with local CT accumulation. Genotype‐specific resistance ranking also depended on the experimental conditions. These results support the hypothesis that growth conditions may affect selection pressures mediated by aphids in accordance with balancing selection theory.