Monarch flycatchers are a major component of Australo-Pacific and Wallacean avifaunas. To date, the family has received incomplete attention by molecular systematists who focused on subclades with minimal character and/or taxon sampling. As a result, Monarchidae taxonomy is still out-of-date, and biogeographic reconstructions have been based on poorly-resolved phylogenies, limiting their interpretation. Here, we produced a comprehensive, molecular phylogeny of the Monarchidae inferred from mitochondrial and nuclear loci using both concatenated and multilocus coalescent frameworks. We sampled 92% of the 99 recognized monarchid biological species and included deeper sampling within several phylogenetic species complexes, including Monarcha castaneiventris, Symposiachrus barbatus, and Terpsiphone rufiventer. Melampitta is identified as sister to the monarch flycatchers, which themselves comprise four major lineages. The first lineage comprises Terpsiphone and allies, the second lineage is Grallina, the third is Arses and Myiagra, and the fourth lineage comprises a diverse assemblage of genera including the “core monarchs” and the most geographically isolated groups like Chasiempis (Hawaii) and Pomarea (eastern Polynesia). Gene tree discordance was evident in Myiagra, which has implications for basal lineages in the genus (e.g., M. azureocapilla, M. hebetior, and M. alecto). Numerous genera within the core monarchs are paraphyletic, including Mayrornis and Pomarea, whereas the validity of others such as Metabolus are questionable. We recognize polytypic taxa as multiple species, including Lamprolia victoriae and Myiagra azureocapilla. In general, the topology of species complexes included short internodes that were not well resolved, owing to their rapid diversification across island archipelagos. Terpsiphone rufiventer comprises multiple lineages, including a heretofore-unappreciated West African lineage, but relationships within these rapid radiations will require extensive genomic sampling for further resolution. This study establishes a new benchmark for Monarchidae systematics and it provides an excellent framework for future work on biogeography and character evolution in a diverse Australo-Papuan radiation.