Interactions between plants and aquatic insects are poorly documented, especially for turbid freshwater ecosystems. Many Swiss lakes offer such habitats, several of which are inhabited by the leaf beetle Macroplea appendiculata (Panzer 1794). This donaciid beetle is the only coleopteran species known to complete its life cycle entirely under water, where it lives primarily on perfoliate pondweed (Potamogeton perfoliatus L.), with Eurasian watermilfoil (Myriophyllum spicatum L.) as an alternative host plant. Direct observations during diving trips, aquatic olfactometer bioassays, and stir bar sorptive extractions (SBSE) coupled with GC–MS analysis were used to understand how these beetles locate their patchily distributed host plants and congeners in a harsh, often swirling environment. In olfactometer assays we observed that the aquatic beetle is strongly attracted to water extracts of pondweed, whereas neither mature males nor females beetles seem to produce attractive cues. The chemical analyses revealed that perfoliate pondweed releases one dominating compound, eucalyptol. Olfactometer assays confirmed that this is a potent attractant for the beetle. We also observed attraction to phytol, which is released by the main, as well as the alternative host plant. These finding are somewhat surprising as eucalyptol has never been reported for aquatic plants and phytol is poorly soluble in water. In addition, both are frequently described as insect repellents in terrestrial ecosystems. We suggest that these terpenoids normally have a defensive function against herbivores and pathogens, but that the highly specialized leaf beetle has evolved to exploit its host’s defence chemistry for optimal foraging.