Microorganisms must distribute their limited resources among different physiological functions, including those that do not directly contribute to growth. In this study, we investigate the allocation of resources to flagellar swimming, the most prominent and biosynthetically costly of such cellular functions in bacteria. Although the growth-dependence of flagellar gene expression in peritrichously flagellated Escherichia coli is well known, the underlying physiological limitations and regulatory strategies are not fully understood. By characterizing the dependence of motile behavior on the activity of the flagellar regulon, we demonstrate that, beyond a critical number of filaments, the hydrodynamics of propulsion limits the ability of bacteria to increase their swimming by synthesizing additional flagella. In nutrient-rich conditions, E. coli apparently maximizes its motility until reaching this limit, while avoiding the excessive cost of flagella production. Conversely, during carbon-limited growth motility remains below maximal levels and inversely correlates with the growth rate. The physics of swimming may further explain the selection for bimodal resource allocation in motility at low average expression levels. Notwithstanding strain-specific variation, the expression of flagellar genes in all tested natural isolates of E. coli also falls within the same range defined by the physical limitations on swimming and its biosynthetic cost.