Among birds, white-eyes (genus Zosterops) have diversified so extensively that Jared Diamond and Ernst Mayr referred to them as the “great speciator”. The Zosterops lineage exhibits some of the fastest rates of species diversification among vertebrates, and its members are the most prolific passerine island colonisers. We present a high-quality genome assembly for the silvereye (Z. lateralis), a white-eye species consisting of several subspecies distributed across multiple islands. We investigate the genetic basis of rapid diversification in white-eyes by conducting genomic analyses at varying taxonomic levels. Firstly, we compare the silvereye genome to those of birds from different families and searched for genomic features that may be unique to Zosterops. Secondly, we compare the genomes of different species of white-eyes from Lifou island (South Pacific), using whole genome re-sequencing and restriction-site associated DNA. Thirdly, we contrast the genomes of two subspecies of silvereye that differ in plumage colour. In accordance with theory, we show that white-eyes have high rates of substitutions, gene duplication and positive selection relative to other birds. Below genus level, we find that genomic differentiation accumulates rapidly and reveal contrasting demographic histories between sympatric species on Lifou, indicative of past interspecific interactions. Finally, we highlight genes possibly involved in colour polymorphism between the subspecies of silvereye. By providing the first whole-genome sequence resources for white-eyes and by conducting analyses at different taxonomic levels, we provide genomic evidence underpinning this extraordinary bird radiation.