Postnatal growth in birds and mammals is the time of highest vulnerability and relatively high energy demands and therefore shapes the organisms future outcomes. Several different factors might impose limitations on growth in juveniles, one of them being the efficiency of the digestive process and size of the gastrointestinal tract. We tested the gut size-growth rate relationship using a unique experimental model - mice from a selection experiment designed to produce two lines with divergent levels of basal metabolic rate (BMR): the high BMR (H-BMR) and low BMR line type (L-BMR). These lines differ not only with respect to BMR, but also correlated traits—internal organ size and food intake. Applying a cross-fostering design and a thermoregulatory burden imposed by shaving the mothers, demonstrated that the mass of intestine strongly affected the growth rate, with the H-BMR pups having larger intestines and growing fastest, and reduced growth rate of pups of both lines nursed by shaved L-BMR mothers. Our study also provides a functional link between high growth rate of neonates and high BMR of adults, partly reflecting metabolic costs of maintenance of their guts.