Nutritional symbiosis between insects and intracellular bacteria (endosymbionts) are a major force of adaptation, allowing animals to colonize nutrient-poor ecological niches. Many beetles feeding on tyrosine-poor substrates rely on a surplus of aromatic amino acids produced by bacterial endosymbionts that synthesize them autotrophically. This surplus of aromatic amino acids is crucial for the biosynthesis of a thick exoskeleton, the cuticle, which is made of a matrix of chitin with proteins and pigments built from the tyrosine-derived 3,4-dihydroxyphenylalanine (DOPA14), providing an important defensive barrier against biotic and abiotic stress. Other endosymbiont-related advantages for beetles include a faster development, and improved fecundity. The association between the cereal weevil Sitophilus oryzae and Sodalis pierantonius endosymbiont19 represents a unique case study: in young adult weevils, endosymbionts undergo a massive proliferation concomitant with the cuticle tanning, then they are fully eliminated. While endosymbiont clearance is a host-controlled process, the mechanism triggering endosymbiont proliferation remains poorly understood. Here, we show that endosymbiont proliferation relies on host carbohydrate intake. Remarkably, insect fecundity was preserved, and the cuticle tanning achieved, even when endosymbiont proliferation was experimentally blocked, except in the context of a severely unbalanced diet. Moreover, a high endosymbiont load coupled with nutrient shortage dramatically impacts host survival, revealing the high energy cost of proliferating endosymbionts and the incapacity of the host to adjust energy allocation.