Bacterial species thrive under a wide variety of conditions. Different species can grow at vastly different rates even for those sharing the same optimal conditions; e.g., Vibrio natriegens grows more than 50% faster than E. coli and B. subtilis in rich medium at 37C. To determine molecular and physiological factors setting the rate of bacterial growth, we employed quantitative proteomics supplemented by measurements of ribosome kinetics to compare the proteome allocation programs of various species chosen across the bacterial phylogeny. We find a nearly identical strategy of allocating ribosomes and biosynthetic enzymes adopted by fast growers despite their very different growth rates and phylogenic distances. In particular, the super-fast growth of V. natriegens arises from fast kinetics of its enzymes, rather than the enzyme amounts. A very different strategy is adopted for slow-growing bacteria such as rhizobium, mycobacterium, and streptomyces. These two distinct strategies can be rationalized by a single evolutionary rule. A plethora of predictions are quantitatively validated.