The arms race between plants and herbivores has resulted in a great diversity of plant compounds to act as defences against attackers. It has concurrently resulted in herbivorous pest adaptations to host defences, including plant-host defence suppression through the action of secreted effectors, and detoxification of phytochemicals ingested during feeding. While these two mechanisms of herbivore adaptation are relatively well studied, they have not been tested for use at the same time. This study uses the model plant species Solanum lycopersicum (tomato), and the model arthropod species Tetranychus urticae (two-spotted spider mite), to characterize the utilization of the above-mentioned mechanisms in an experimental adaptation set-up. Two spider mite strains, non-adapted (ancestral) and tomato-adapted, were used to infest tomato under different experimental conditions to interrogate the adaptation process. Tomato adaptation was validated through plant damage and mite performance assays. Transcriptional analysis of differentially expressed genes demonstrated an attenuation of the response to non-adapted mites by adapted ones, indicating the defence response to be deficient in induced defence programs, such as jasmonic acid biosynthesis and protease inhibitor biosynthesis. This was supported with marker gene and hormone quantification. However, inhibition activity was found to be differentially induced in different tomato cultivars, being highly induced in Moneymaker and attenuated in Heinz samples fed on by adapted mites, suggesting mites still encounter protease inhibitors as a plant defence in certain tomato cultivars despite being adapted to tomato in general. A mite co-infestation experiment was used to demonstrate that any benefit to host-plant modulation occurs only at the feeding site. Characterization of mite protease activity and fecundity post-inhibition by a synthetic inhibitor, E-64, suggest that mites increase their protease activity to overcome tomato protease inhibitors. Detoxification was also found to be involved in tomato adaptation, whereby inhibiting different classes of enzymes (cytochrome P450s, esterases, or glutathione-S-transferases) resulted in decreased fecundity on tomato