Traits of chemically-defended animals can change as an individual grows and matures, and both theoretical and empirical evidence favour a direction of change from crypsis to aposematism. This study examines the suite of traits involved in an unusual opposite shift from aposematism to crypsis in a neotropical toxic-plant-feeding Romaleid grasshopper, Chromacris psittacus (Gerstaecker, 1873). Field surveys, behavioural observations and a rearing experiment compare host plant choice, aggregation, locomotion and thermoregulation between life history stages. Results showed that both nymphs and adults fed exclusively on a narrow range of Solanaceae plants, suggesting that the shift in defensive syndrome is not due to a change in chemical defense. Instead, nymphal aposematism appears linked to aggregation in response to plant-based selection pressures. Slow nymphal development suggests a cost to feeding on toxic plant compounds, and grouping could mitigate this cost. Grouping also increases conspicuousness, and hence can favour warning colourating in chemically-defended insects. The role of diet breadth in aposematism is poorly understood, and these results suggest how constraints imposed by feeding on toxic plants can generate bottom-up selection pressures shaping the adaptive suites of traits of chemically-defended animals.