The honeyeaters are the most species-rich clade of birds east of Wallace’s Line. They occupy a wide range of habitats, from desert to rainforest, and occur throughout Australia, New Guinea, and oceanic islands across Wallacea and the Pacific. Honeyeater natural history is well characterised, but comparative studies of this group are hampered by the lack of a well-supported phylogeny. Here, we infer the first genome-scale, genus-level phylogeny of the honeyeaters using 4397 ultraconserved elements from 57 species. We analysed the data using concatenated and species-tree approaches, and we found support for novel clades previously undetected in analyses of single- or multi-locus datasets. Despite sequencing thousands of loci, phylogenetic relationships of the New Caledonian Crow Honeyeater (Gymnomyza aubryana) remain equivocal. This study provides a new phylogenetic framework from which to study the ecology and evolution of one of Australasia’s most iconic avian clades.