Significance Fungus-cultivating termites are icons of ecologically successful herbivores in (sub)tropical ecosystems, cultivating Termitomyces fungi for overcoming the rigid lignin barrier of wood resources. To date, research on these ectosymbiotic fungi has only identified laccases, rather than the typical ligninolytic peroxidases. Using 2D gel-state NMR, we chemically tracked the fate of lignin from the original poplar wood throughout the complex food-processing system in a farming termite. We found young worker termites rapidly depolymerize and degrade even the most recalcitrant wood lignin structures, facilitating polysaccharide cleavage by symbiotic fungi. These results suggest that the natural systems for lignin degradation/pretreatment are far beyond the systems currently recognized and are potential sources of novel ligninolytic agents, enabling more efficient plant cell wall utilization.