Nutrition has far‐reaching effects on both the ecology and evolution of species. A substantial body of work has examined the role of host plant quality on insect herbivores, with a particular focus on specialist–generalist dynamics, the interaction of growth and other physiological attributes on fitness and tritrophic effects. Measures of plant quality usually involve one or two axes of nutritional space: typically secondary metabolites or elemental proxies (N and C) of protein and carbohydrates, respectively.Here, we describe the nutrient space of seven host plants of the specialist insect herbivore, Manduca sexta, using an approach that measures physiologically relevant sources of nutrition, soluble protein and digestible carbohydrates. We show that plant species differ markedly in their nutrient content, offering developing insect herbivores a range of available nutrient spaces that also depend on the age of the leaves being consumed.The majority of host‐plant species produce diets that are suboptimal to the herbivore, likely resulting in varying levels of compensatory feeding for M. sexta to reach target levels of protein to ensure successful growth and development. Low‐quality diets can also impact immune function leading to complex patterns of optimization of plant resources that maximizes both growth and the ability to defend from parasitoids and pathogens. This study is the first to quantify the nutrient space of a suite of host plants used by an insect herbivore using physiologically relevant measures of nutrition.