Deletion rates are thought to be important factors in determining the genome size of organisms in nature. Although it is indisputable that deletions, and thus deletion rates, affect genome size, it is unclear how, or indeed if, genome size is regulated via the deletion rate. Here, we employ a mathematical model to determine the evolutionary fate of deletion rate mutants. Simulations are employed to explore the interactions between deletions, deletion rate mutants, and genome size. The results show that, in this model, the fate of deletion rate mutants will depend on the fraction of essential genomic material, on the frequency of sexual recombination, as well as on the population size of the organism. We find that there is no optimal deletion rate in any state. However, at one critical coding density, all changes in deletion rate are neutral and the rate may drift either up or down. As a consequence, the coding density of the genome is expected to fluctuate around this critical density. Characteristic differences in the impact of deletion rate mutations on prokaryote and eukaryote genomes are described.