Clownfishes are an iconic group of coral reef fishes that evolved a mutualistic interaction with sea anemones, which triggered the rapid diversification of the group. Following the emergence of this mutualism, clownfishes diversified into different ecological niches and developed convergent phenotypes associated with their host use. The genetic basis of the initial acquisition of the mutualism with host anemones has been described, but the genomic architecture underlying clownfish diversification once the mutualism was established and the extent to which clownfish phenotypic convergence originated through shared genetic mechanisms are still unknown. Here, we investigated these questions by performing comparative genomic analyses on the available genomic data of five pairs of closely related but ecologically divergent clownfish species. We found that clownfish diversification was characterized by bursts of transposable elements, an overall accelerated coding evolution, incomplete lineage sorting, and ancestral hybridization events. Additionally, we detected a signature of positive selection in 5.4% of the clownfish genes. Among them, five presented functions associated with social behavior and ecology, and they represent candidate genes involved in the evolution of the size-based hierarchical social structure so particular to clownfishes. Finally, we found genes with patterns of either relaxation or intensification of purifying selection and signals of positive selection linked with clownfish ecological divergence, suggesting some level of parallel evolution during the diversification of the group. Altogether, this work provides the first insights into the genomic substrate of clownfish adaptive radiation and integrates the growing collection of studies investigating the genomic mechanisms governing species diversification.