Sea urchins have the capacity to destructively overgraze kelp beds and cause a wholesale shift to an alternative and stable ‘urchin barren’ state. However, their destructive grazing behaviour can be highly labile and contingent on behavioural shifts at the individual and local population level. Changes in supply of allochthonous food sources, i.e. availability of drift-kelp, is often suggested as a proximate trigger of change in sea urchin grazing behaviour, yet field tests of this hypothesis are rare. Here we conduct a suite of in situ behavioural surveys and manipulative experiments within kelp beds and on urchin barrens to examine foraging movements and evidence for a behavioural switch to an overgrazing mode by the Australian sea urchin Heliocidaris erythrogramma (Echinometridae). Tracking of urchins using time-lapse photography revealed urchin foraging to broadly conform to a random-walk-model within both kelp beds and on barren grounds, while at the individual level there was a tendency towards local ‘homing’ to proximate crevices. However, consistent with locally observed ‘mobile feeding fronts’ that can develop at the barrens-kelp interface, urchins were experimentally inducible to show directional movement toward newly available kelp. Furthermore, field assays revealed urchin grazing rates to be high on both simulated drift-kelp and attached kelp thalli on barren grounds, however drift-kelp but not attached kelp was consumed at high rates within kelp beds. Time-lapse tracking of urchin foraging before/ after the controlled addition of drift-kelp on barrens revealed a reduction in foraging movement across the reef surface when drift-kelp was captured. Collectively results indicate that the availability of drift-kelp is a pivotal trigger in determining urchin feeding modes, which is demonstrably passive and cryptic in the presence of a ready supply of drift-kelp. Recovery of kelp beds therefore appears possible if a sustained influx of drift-kelp was to inundate urchin barrens, particularly on reefs where local urchin densities and where grazing pressure is close to the threshold enabling kelp bed recovery.