Glandular trichomes (GT) are specialized cell factories that have the capacity to produce large amounts of metabolites which can amount to over 10% of the leaf dry weight. The specific expression of secondary metabolite pathways in glandular trichomes has facilitated their elucidation. However, little is known about the connection between central carbon and specialized metabolism in these cells. To address this question, we used the type VI glandular trichomes from a cultivated (Solanum lycopersicum LA4024) and a wild tomato accession (Solanum habrochaites LA1777) as a model. Our study is based on metabolomics, transcriptomics, proteomics and 13C-labeling datasets of trichome and leaves samples. This comparative analysis allowed us to identify specific features of trichomes in comparison to leaves. Tomato type VI trichomes are photosynthetic but acquire their carbon essentially from the leaves in the form of sucrose. Relatively high expression levels of photosystem genes and comparatively low expression of Calvin-cycle and photorespiration genes indicate that photosynthesis is used primarily to produce energy and reducing power to drive the high metabolic activity. High levels of polyunsaturated fatty acids, oxylipins, and of oxidized glutathione and high transcript and protein levels of associated enzymes further indicate a distinct capacity of GT to cope with oxidative stress. Enzymes which are involved in the supply of key precursors for the production of terpenoids both from the cytosol and in the chloroplasts are markedly increased. Finally, some enzymes that are typically associated with C4-photosynthesis are highly expressed in trichomes, suggesting that CO2 recycling processes may increase the efficiency of C usage in these cells. Based on this information we propose a model on how the glandular trichomes achieve high metabolic efficiency.