Insect attack frequently down-regulates photosynthetic proteins. To understand how this influences the plant-insect interaction, we transformed Nicotiana attenuata to independently silence ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCase) activase (RCA) and RuBPCase and selected lines whose photosynthetic capacity was similarly reduced. Decreases in plant growth mirrored the decreases in photosynthesis, but the effects on herbivore performance differed. Both generalist (Spodoptera littoralis) and specialist (Manduca sexta) larvae grew larger on RCA-silenced plants, which was consistent with decreased levels of trypsin protease inhibitors and diterpene glycosides and increased levels of RuBPCase, the larvae's main dietary protein. RCA-silenced plants were impaired in their attack-elicited jasmonate (JA)-isoleucine (Ile)/leucine levels, but RuBPCase-silenced plants were not, a deficiency that could not be restored by supplementation with Ile or attributed to lower transcript levels of JAR4/6, the key enzyme for JA-Ile conjugation. From these results, we infer that JA-Ile/leucine signaling and the herbivore resistance traits elicited by JA-Ile are influenced by adenylate charge, or more generally, carbon availability in RCA- but not RuBPCase-silenced plants. Growth of generalist larvae on RuBPCase-silenced plants did not differ from growth on empty vector controls, but the specialist larvae grew faster on RuBPCase-silenced plants, which suggests that the specialist can better tolerate the protein deficiency resulting from RuBPCase silencing than the generalist can. We conclude that the plant-herbivore interaction is more influenced by the particular mechanisms that reduce photosynthetic capacity after herbivore attack than by the magnitude of the decrease, which highlights the value of understanding defense mechanisms in evaluating growth-defense tradeoffs.