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• Populus genotypes with low tannin concentrations experienced higher Venturia infection. • Nitrogen enrichment caused Venturia infection to become more frequent. • Genotypes with high tannin defenses were able to grow taller in response to nitrogen enrichment. Boreal forests receive nitrogen-(N)-enrichment via atmospheric deposition and industrial fertilization. While it is known that N-enrichment can intensify interactions with natural antagonists, it remains poorly understood how genetic variability in plant defense chemistry can affect biotic interactions and height growth in N-enriched environments. We grew replicates of five low- and high-tannin Populus tremula genotypes, respectively, under three N-treatments (ambient, 15, and 150 kg N ha−1 yr−1). We assessed shoot blight occurrence (i.e. symptoms caused by Venturia fungi) during four growing seasons, and tree height growth during the same period. Damage by Venturia spp. increased with N-addition during all years, likely due to enhanced foliar quality. Low–tannin plants showed higher incidences of Venturia infection than high-tannin plants, regardless of the N-input-level. Height responded to an N-by-tannin-group interaction, which occurred because high-tannin plants grew taller than low-tannin plants at the high N-treatment, but not under the other N-levels. This pattern indicates that innate resource investment into tannin production yields a positive effect on growth under N-enriched conditions. Given that N-deposition is increasing globally, our research suggests that further studies are needed to investigate how N-enrichment interacts with plant defense traits globally. Moreover, our research suggests that N-deposition may provide an advantage for well-defended, high-tannin plants; and further, that genetic diversity in plant defense may be a key mechanism by which plant populations respond to this change. [ABSTRACT FROM AUTHOR]