A tenet of life history evolution is that allocation of limited resources results in trade-offs, such as that between reproduction and lifespan. Reproduction and lifespan are also influenced proximately by differences in the availability of specific nutrients. What is unknown is how the evolution of the ability to use a nutritionally novel diet is reflected in this fundamental trade-off. Does the evolution of the ability to use a nutritionally novel food maintain the trade-off in reproduction and longevity, or do the proximate effects of nutrition alter the adapted trade-off? We tested this by measuring trade-offs in male milkweed bugs, Oncopeltus fasciatus, fed either an adapted diet of sunflower or the ancestral diet of milkweed. Sunflower-fed males lived longer but invested less in reproduction, both in mating and fertility. Milkweed-fed males invested in both mating and fertility at the expense of survival. The evolution of an expanded diet was not constrained by the existing trade-off, but instead was accompanied by a different trade-off between reproduction and longevity. We suggest that this occurs because diets differ in promoting germ line development or longevity.