Commiphora (Burseraceae) is the most species-rich genus in the frankincense and myrrh family, whose widespread and often remote distribution in seasonally dry tropical forests globally has impeded efforts to resolve its taxonomy and investigate its systematic biology. Here we focus on establishing the origin and evolution of Commiphora species native to Madagascar, all of which are endemic. Recent work has uncovered 16 new Malagasy species, bringing the total number of island endemic species to 44 and comprising nearly 25% of the genus. Previous phylogenetic studies of Commiphora have indicated that Malagasy lineages immigrated to and radiated within the island twice. We test this biogeographic hypothesis more thoroughly using a nearly comprehensive sampling of species from Madagascar, an expanded sampling of Commiphora species native to other regions, and a greater depth of DNA sequence data from the nuclear (nrETS, nrITS) and chloroplast (psbA-trnH, ndhF-rpl32, and trnD—trnT) genomes. Results from this expanded phylogenetic analysis include strong support for seven infrageneric clades within a monophyletic Commiphora, which we refer to as the ‘Lasiodisca,’ ‘Granulifera,’ ‘Saxicola,’ ‘Gariepensis,’ ‘Spinescens,’ ‘Arafy,’ and ‘Rhynchocarpa’ clades. Malagasy species comprise four distantly related lineages, including one species sister to all other Commiphora species (C. lasiodisca), the species-rich ‘Arafy,’ and ‘Rhynchocarpa’ clades, and one species embedded within the predominantly East African ‘Spinescens’ clade (C. simplicifolia). We describe the morphological and geographic affinities of each infrageneric and Malagasy lineage and identify priorities for future systematic study of the genus.