Infection with the necrotrophic fungus Diplodia sapinea is among the economically and ecologically most devastating diseases of conifers in the northern hemisphere accelerated by global climate change. The present study aims to characterize the changes mediated by D. sapinea infection on its pine host (Pinus sylvestris L.) that lead to the death of its needles. For this purpose, we performed an indoor infection experiment and inoculated shoot tips of pine seedlings with virulent D. sapinea. The consequences for foliar traits, including the phytohormone profile were characterized at both the metabolite and transcriptome level. Our results showed that D. sapinea infection strongly affected foliar levels of most phytohormones and impaired a multitude of other metabolic and structural foliar traits, such as ROS scavenging. Transcriptome analysis revealed that these changes are partially mediated via modified gene expression by fungal exposure. D. sapinea appears to overcome defense reactions of its pine host by reprogramming gene expression and post-transcriptional controls that determine essential foliar metabolic traits such as the phytohormone profile, cell wall composition and antioxidative system.