In insects, lifespan and reproduction are strongly associated with nutrition. The ratio and amount of nutrients individuals consume affects their life expectancy and reproductive investment. The geometric framework (GF) enables us to explore how animals regulate their intake of multiple nutrients simultaneously and determine how these nutrients interact to affect life history traits of interest. Studies using the GF on host-generalist tephritid flies have highlighted trade-offs between longevity and reproductive effort in females, mediated by the protein to carbohydrate (P:C) ratio that individuals consume. Here, we tested how P and C intake affect lifespan (LS) in both sexes, and female lifetime (LEP) and daily (DEP) egg production, in Ceratitis cosyra, a host-specialist tephritid fly. We then determined the P:C ratio that C. cosyra defends when offered a choice of foods. Female LS was optimised at a 0:1 P:C ratio whereas to maximise their fecundity females needed to consume a higher P:C ratio (LEP = 1:6 P:C; DEP = 1:2.5 P:C). In males, LS was also optimised at a low P:C ratio of 1:10. However, when given the opportunity to regulate their intake, both sexes actively defended a 1:3 P:C ratio, which is closer to the target for DEP than either LS or LEP. Our results show that female C. cosyra experienced a moderate trade-off between LS and fecundity. Moreover, the diets that maximised expression of LEP and DEP were of lower P:C ratio than those required for optimal expression of these traits in host-generalist tephritids or other generalist insects.