The West Indian avifauna has provided fundamental insights into island biogeography, taxon cycles, and the evolution of avian behavior. Our interpretations, however, rely on robust hypotheses of evolutionary relationships and consistent conclusions about taxonomic status in groups with many endemic island populations. Here we present a phylogenetic study of the West Indian thrashers, tremblers, and allies, an assemblage of at least 5 species found on 29 islands, which is considered the archipelago’s only avian radiation. We improve on previous phylogenetic studies of this group by using double-digest restriction site-associated DNA sequencing (ddRAD-seq) to broadly sample loci scattered across the nuclear genome. A variety of analyses, based on either nucleotide variation in 2,223 loci that were recovered in all samples or on 13,282 loci that were confidently scored as present or absent in all samples, converged on a single well-supported phylogenetic hypothesis. In contrast to previous studies, we found that the resident West Indian taxa form a monophyletic group, exclusive of the Neotropical-Nearctic migratory Gray Catbird Dumetella carolinensis, which breeds in North America. Earlier studies indicated that the Gray Catbird was nested within a clade of island resident species. Instead, our findings imply a single colonization of the West Indies without the need to invoke a subsequent ‘reverse colonization’ of the mainland by West Indian taxa. Furthermore, our study is the first to sample both endemic subspecies of the endangered White-breasted Thrasher Ramphocinclus brachyurus. We find that these subspecies have a long history of evolutionary independence with no evidence of gene flow, and are as genetically divergent from each other as other genera in the group. These findings support recognition of R. brachyurus (restricted to Martinique) and the Saint Lucia Thrasher R. sanctaeluciae as two distinct, single-island endemic species, and indicate the need to re-evaluate conservation plans for these taxa. Our results demonstrate the utility of phylogenomic datasets for generating robust systematic hypotheses.