Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation involving a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, contrasting our understanding of how adaptive and neutral processes shaped genome evolution across their radiation. Here, we build new, highly contiguous genome assemblies for nine new Heliconiini, reference-assembled genomes for 29 species, and improve 10 existing assemblies, to provide a major new dataset of annotated genomes for 63 species, including 58 species within the Heliconiini tribe. We provide a robust, dated heliconiine phylogeny, identify major patterns of introgression, explore the evolution of genome size, content, and the genomic basis of key innovations in this enigmatic group for the first time. We illustrate how dense genomic sampling improves our resolution of gene-phenotype links, and our understanding of how genomes evolve.