Abstract Molecular phylogenetics has fundamentally altered our understanding of the taxonomy, systematics and biogeography of corals. Recently developed phylogenomic techniques have started to resolve species-level relationships in the diverse and ecologically important genus Acropora, providing a path to resolve the taxonomy of this notoriously problematic group. We used a targeted capture dataset (2032 loci) to investigate systematic relationships within an Acropora clade containing the putatively widespread species Acropora tenuis and its relatives. Using maximum likelihood phylogenies and genetic clustering of single nucleotide polymorphisms from specimens, including topotypes, collected across the Indo-Pacific, we show ≥ 11 distinct lineages in the clade, only four of which correspond to currently accepted species. Based on molecular, morphological and geographical evidence, we describe two new species; Acropora rongoi n. sp. and Acropora tenuissima n. sp. and remove five additional nominal species from synonymy. Systematic relationships revealed by our molecular phylogeny are incongruent with traditional morphological taxonomy and demonstrate that characters traditionally used to delineate species boundaries and infer evolutionary history are homoplasies. Furthermore, we show that species within this clade have much smaller geographical ranges and, consequently, population sizes than currently thought, a finding with profound implications for conservation and management of reef corals.