Background: Across all sequenced bacterial genomes, the number of domains n in different functional categories c scales as a power-law in the total number of domains n, i.e. n ∝n with exponents α that vary across functional categories. Here we investigate the implications of these scaling laws for the evolution of domain-content in bacterial genomes and derive the simplest evolutionary model consistent with these scaling laws. Results: We show that, using only an assumption of time invariance, the scaling laws uniquely determine the relative rates of domain additions and deletions across all functional categories and evolutionary lineages. In particular, the model predicts that the rate of additions and deletions of domains of category c is proportional to the number of domains n currently in the genome and we discuss the implications of this observation for the role of horizontal transfer in genome evolution. Second, in addition to being proportional to n, the rate of additions and deletions of domains of category c is proportional to a category-dependent constant ρ, which is the same for all evolutionary lineages. This 'evolutionary potential' ρ represents the relative probability for additions/deletions of domains of category c to be fixed in the population by selection and is predicted to equal the scaling exponent α. By comparing the domain content of 93 pairs of closely-related genomes from all over the phylogenetic tree of bacteria, we demonstrate that the model's predictions are supported by available genome-sequence data. Conclusion: Our results establish a direct quantitative connection between the scaling of domain numbers with genome size, and the rate of addition and deletions of domains during short evolutionary time intervals.