Although recent research has revealed high genomic complexity in the earliest-splitting animals and their ancestors, the macroevolutionary trends orchestrating gene repertoire evolution throughout the animal phyla remain poorly understood. We used a phylogenomic approach to interrogate genome evolution across all animal phyla. Our analysis uncovered a bimodal distribution of recruitment of orthologous genes, with most genes gained very 'early' (that is, at deep nodes) or very 'late', representing lineage-specific acquisitions. The emergence of animals was characterized by high values of gene birth and duplications. Deuterostomes, ecdysozoans and Xenacoelomorpha were characterized by no gene gain but rampant differential gene loss. Genes considered as animal hallmarks, such as Notch/Delta, were convergently duplicated in all phyla and at different evolutionary depths. Genes duplicated in all nodes from Metazoa to phylum-specific levels were enriched in functions related to the neural system, suggesting that this system has been continuously and independently reshaped throughout evolution across animals. Our results indicate that animal genomes evolved by unparalleled gene duplication followed by differential gene loss, and provide an atlas of gene repertoire evolution throughout the animal tree of life to navigate how, when and how often each gene in each genome was gained, duplicated or lost.