Plants synthesize diverse specialized metabolites under tissue- and context-specific regulation, yet it remains unclear how tissue-specific herbivory shapes pre- and post-attack metabolomes within each tissue. Using untargeted metabolomics, we compared constitutive and tissue-specific herbivory-induced states across tissues of Capsella bursa-pastoris, a cosmopolitan weed. Profiles separated mainly by tissue; roots had the most constitutive tissue-specific features. Herbivory increased between-tissue dissimilarity, and stems showed the largest set of induced features. The top herbivore-induced stem feature was constitutively higher in roots, consistent with tissue-specific biosynthetic control. Multi-omic evidence indicates a hydrolyzed glucosinolate derivative that may contribute to resistance against root specialists, underscoring adaptive diversification and tissue-specific regulation of specialized-metabolite pathways.