Since volatile organic compounds (VOCs) shape plant defenses against pests, ecologists strive to understand their sources of variation. The worldwide distribution of tomato offers an ideal system to explore the ecological diversity of VOCs produced by plants supporting a large range of local adaptations. In this study, we analyzed the diversity of VOC profiles released by 29 accessions of tomato belonging to five species with different natural histories and including domesticated plants and wild relatives. In addition, olfactometer assays were performed on 10 accessions characterized by strong differences in VOC emissions to test the consequences on host-plant location by a major specialist pest of solanaceous plants, Tuta absoluta. Based on 77 VOCs detected, our results suggest that the large diversity of volatile profiles reflect different biogeographic areas. A phylogenetic tree was constructed to test phylogenetic drivers in VOC emissions. The richness of volatile profiles and sesquiterpenoid emissions were relatively high in ancestral branches and decreased exponentially with evolution according to early-burst patterns. In olfactometer assays, we identified four repellent accessions belonging to S. pennellii, S. habrochaites and S. cheesmaniae. This study points out the importance of inter- and intra-specific diversity of VOCs in antixenosis. Further, our results suggest that methyl salicylate, β-myrcene and sesquiterpenoids such as (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene or α-curcumene could serve as repellents against T. absoluta. In a greenhouse, we confirmed the biological relevance of agroecological research interested in screening repellent plants. Bridging chemical ecology with phylogenetic approaches helps to better understand the evolution of mechanisms supporting anti-herbivore plant defenses.