Monoterpenes are molecules with insecticide properties whose mechanism of action is, however, not completely elucidated. Furthermore, they seem to be able to modulate the monoaminergic system and several behavioural aspects in insects. In particular, tyramine (TA) and octopamine (OA) and their associated receptors orchestrate physiological processes such as feeding, locomotion and metabolism. Here, we show that monoterpenes not only act as biopesticides in Drosophila species but also can cause complex behavioural alterations that require functional type 1 tyramine receptors (TAR1s). Variations in metabolic traits as well as locomotory activity were evaluated in both Drosophila suzukii and Drosophila melanogaster after treatment with three monoterpenes. A TAR1-defective D. melanogaster strain (TAR1PL00408) was used to better understand the relationships between the receptor and monoterpene-related behavioural changes. Immunohistochemistry analysis revealed that, in the D. melanogaster brain, TAR1 appeared to be mainly expressed in the pars intercerebralis, lateral horn, olfactory and optic lobes and suboesophageal ganglion lobes. In comparison to wild-type D. melanogaster, the TAR1PL00408 flies showed a phenotype characterized by higher triglyceride levels and food intake as well as lower locomotory activity. The monoterpenes, tested at sublethal concentrations, were able to induce a downregulation of the TAR1 coding gene in both Drosophila species. Furthermore, monoterpenes also altered the behaviour in wild-type D. suzukii and D. melanogaster 24 h after continuous monoterpene exposure. Interestingly, they were ineffective in modifying the physiological performance of TAR1-defective flies. In conclusion, it appears that monoterpenes not only act as biopesticides for Drosophila but also can interfere with Drosophila behaviour and metabolism in a TAR1-dependent fashion.