Many herbivores sequester plant toxins, and this occurs along a gradient of specialization including “toxic plant generalists” that also consume non-toxic hosts. We hypothesized that availability of toxins for sequestration may trade off with nutritional quality to shape dietary choices in a Lygaeid bug. In the absence of toxins (cardenolides) from a preferred food (milkweed seeds), bugs increased feeding on nutritionally poor, but cardenolide-rich milkweed plant tissue, corresponding to lower growth but greater sequestration. While bugs feeding on only milkweed plant tissue sequestered lower cardenolides than those feeding on seeds, they sequestered more diverse and less polar compounds. Cardenolide production was also induced by feeding on plant tissues, which may have downstream effects on future herbivory and sequestration. Accordingly, sequestration is a driver of diet choice in this toxic plant generalist, even at the cost of feeding on nutritionally poor plant tissue; reciprocally, plants defensively respond to such feeding choices.