The objective of this study was to evaluate the contribution of evolutionary history to variation in the biomass stoichiometry and underlying biochemical allocation patterns of heterotrophic marine bacteria. We hypothesized that phylogeny significantly constrains biochemical allocation strategy and elemental composition among taxa of heterotrophic marine bacteria. Using a ‘common-garden’ experimental design, we detected significant interspecific variation in stoichiometry, macromolecule allocation and growth rate among 13 strains of marine Proteobacteria. However, this variation was not well explained by 16S rRNA phylogenetic relationships or differences in growth rate. Heterotrophic bacteria likely experience C-limitation when consuming resources in Redfield proportions, which consequently decouples growth rate from allocation to rRNA and biomass P content. Accordingly, overall bacterial C : nutrient ratios (C : P = 77, C : N = 4.9) were lower than Redfield proportions, whereas the average N : P ratio of 17 was consistent with the Redfield ratio. Our results suggest that strain-level diversity is an important driver of variation in the C : N : P ratios of heterotrophic bacterial biomass and that the potential importance of non-nucleic acid pools of P warrants further investigation. Continued work clarifying the range and controls on the stoichiometry of heterotrophic marine bacteria will help improve understanding and predictions of global ocean C, N and P dynamics.