Technical Abstract: 1. Leaf-herbivore attack often triggers induced resistance in plants. However, certain specialist herbivores can also take advantage of the induced metabolic changes. In some cases, they even manipulate plant resistance, leading to a phenomenon called induced susceptibility. Compared to above-ground plant-insect interactions, little is known about the prevalence and consequences of induced responses below ground. 2. A recent study suggested that feeding by the specialist root herbivore Diabrotica virgifera virgifera makes maize roots more susceptible to conspecifics. To better understand this phenomenon, we conducted a series of experiments to study the behavioral responses and elucidate the underlying biochemical mechanisms. 3. We found that D. virgifera benefited from feeding on a root system in groups of intermediate size, whereas its performance was reduced in large groups. Interestingly, the herbivore was able to select host plants with an optimal density of conspecifics by using the induced plant volatile (E)-ß-caryophyllene in a dose-dependent manner. Using a split root experiment, we show that the plant induced-susceptibility is systemic and, therefore, plant-mediated. Chemical analyses on plant resource reallocation and defenses upon herbivory showed that the systemic induced-susceptibility is likely to stem from a combination of (i) increased free amino acid concentrations and (ii) relaxation of defense inducibility. 4. These findings show that herbivores can use induced plant volatiles in an optimal, density dependent manner, to aggregate on a host plant and change its metabolism to their own benefit. Our study furthermore helps to explain the remarkable ecological success of D. virgifera in maize fields around the world.