Metabolic control analysis has revealed that flux through pathways is the consequence of system properties, i.e. shared control by multiple steps, as well as the kinetic effects of various pathways and processes over each other. This implies that the allometric scaling of flux rates must be understood in terms of properties that pertain to the regulation of flux rates. In contrast, proponents of models considering the scaling of branching or fractal-like systems suggest that supply rates determine metabolic rates. Therefore, the allometric scaling of supply alone provides a sufficient explanation for the allometric scaling of metabolism. Examination of empirical data from the literature of comparative physiology reveals that basal metabolic rates (BMR) are driven by rates of energy expenditure within internal organs and that the allometric scaling of BMR can be understood in terms of the scaling of the masses and metabolic rates of internal organs. Organ metabolic rates represent the sum of tissue metabolic rates while, within tissues, cellular metabolic rates are the outcome of shared regulation by multiple processes. Maximal metabolic rates (MMR, measured as maximum rates of O2 consumption, VO2max) during exercise also scale allometrically, are also subject to control by multiple processes, but are due mainly to O2 consumption by locomotory muscles. Thus, analyses of the scaling of MMR must consider the scaling of both muscle mass and muscle energy expenditure. Consistent with the principle of symmorphosis, allometry in capacities for supply (the outcome of physical design constraints) is observed to be roughly matched by allometry in capacities for demand (i.e. for energy expenditure). However, physiological rates most often fall far below maximum capacities and are subject to multi-step regulation. Thus, mechanistic explanations for the scaling of BMR and MMR must consider the manner in which capacities are matched and how rates are regulated at multiple levels of biological organization.