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With reciprocal rearing experiments, we tested the hypothesis that adaptive differences in host-use traits among soapberry bug populations have a genetic basis. These experiments were conducted with two host races from Florida, an ‘ancestral-type’ one on a native host plant species and a ‘derived’ one on a recently introduced plant species (colonized mainly post-1950), on whose seed crops this insect depends for growth and reproduction. Compared to the native host species, the introduced host produces larger seed crops over a much briefer annual period. Its seeds are also significantly higher in lipids and lower in nitrogen. The bug populations exhibit greater juvenile survivorship on their ‘home’ hosts; that is, the derived population survives better on seeds of the introduced host than does its ancestral-type counterpart, and vice versa. Regardless of the rearing host, populations from the introduced host lay much smaller eggs, and fecundity measures show a more complex pattern than does survivorship: the ancestral-type population produces eggs at the same rate on each host, while the derived population is less fecund on the native host and exhibits enhanced fecundity on the introduced host. These results indicate that the population differences are evolved rather than host-induced. They appear to be adaptive responses to host differences in the spatial and temporal distribution of seed availability and nutritional quality, and show that increased performance on the alien host has evolved with surprising speed and magnitude, with concomitant reductions in performance on the original host.