The purpose of this study was to better understand the interactive impact of two soil-borne pathogens, Phytophthora cactorum (as the primary pathogen) and Armillaria gallica (as secondary), on two-year-old seedlings of silver birch (Betula pendula) subjected to stress caused by mechanical defoliation simulating primary insect feeding. One year after treatments, the chlorophyll fluorescence measurement and gas chromatography coupled with mass spectrometry (GC-MS) were used to analyze the photosynthetic activity in leaves, the volatile organic compounds (VOCs) emitted by birch leaves and chemical compounds from roots. Only the infection of roots by P. cactorum increased photosynthetic rates in the leaves, which may suggest its cryptic development in contrast to fungi. The birch leaves in seedlings exposed to 50% defoliation, inoculation with P. cactorum and A. gallica emitted more aromatic carbonyls and alcohols, as well as half as much aliphatic esters, compared to untreated controls. In infected birch roots, the production of phenols, triterpenes and fatty alcohols increased, but fatty acids decreased. This was the first experimental confirmation of the pathogenicity of P. cactorum on silver birch seedlings in Poland. The most severe damage to roots took place only in the case of two-way or three-way interactions. Higher levels of aromatic carbonyls and alcohols in leaves, as well as phenolic compounds in roots of stressed birches (compared to control) suggest an activation of plant systemic acquired resistance (SAR).