Purpose The woolly beech aphid thrives on European beech leaves, which has complex direct and indirect impacts on above- and belowground processes. A mechanistic understanding of insect-mediated changes in organic carbon (OC) availability for microbial life and its implications for element cycling is still lacking. This study aims at disentangling aphid-induced effects on phyllosphere and rhizosphere bacterial communities, as well as investigating feedbacks to OC transfer from the canopy to the mineral soil. Methods Following 2.5 months of infestation, we tracked the fate of OC ( 13 CO 2 pulse-labelling) in several compartments of beech sapling – soil mesocosms over 5 days. In ecosystem solutions, water extracts and soil/plant compartments we determined OC and N and solid δ 13 C. Bacterial community structure (16S rRNA gene targeted amplicon sequencing and quantitative PCR) and metabolite profiles (LC-qTOF-MS) were analysed. Results We found significantly higher aphid-mediated inputs of OC within throughfall. Honeydew-derived C on infested leaves was inconsequential for total phyllosphere bacterial abundances, but verifiably affected the community structure. In all soil compartments, cold-water extractable OC pools declined significantly by frequent inputs of readily available OC. This pattern might relate to reductions in rhizodepositions and altered microbial processing by accelerated soil C-mineralization. As a result, the abundance of metabolites changed significantly in different ecosystem solutions. Conclusions Our findings attest that insect infestations induce distinct direct and indirect effects on plant-insect-microbiome interactions leading to marked alterations in C dynamics. This integrated approach improves our understanding on microbial dynamics and biogeochemistry and evaluates the role of insects for ecosystem processes.