In RNA viruses, which have high mutation—and fast evolutionary— rates, gene overlapping (i.e., genomic regions that encode more than one protein) is a major factor controlling mutational load and therefore the virus evolvability. Although DNA viruses use host high-fidelity polymerases for their replication, and therefore should have lower mutation rates, it has been shown that some of them have evolutionary rates comparable to those of RNA viruses. Notably, these viruses have large proportions of their genes with at least one overlapping instance. Hence, gene overlapping could be a modulator of virus evolution beyond the RNA world. To test this hypothesis, we use the genus Begomovirus of plant viruses as a model. Through comparative genomic approaches, we show that terminal gene overlapping decreases the rate of virus evolution, which is associated with lower frequency of both synonymous and nonsynonymous mutations. In contrast, terminal overlapping has little effect on the pace of virus evolution. Overall, our analyses support a role for gene overlapping in the evolution of begomoviruses and provide novel information on the factors that shape their genetic diversity.