Antennaria are dioecious perennial herbs distributed mainly in the Holarctic Region, with their major center of diversity in the Rocky Mountains of Western North America. The genus comprises 33 known sexual diploid/tetraploid species and at least five polyploid agamic complexes which mostly reproduce by forming asexual seeds. We performed a phylogenetic reconstruction of the 31 sexually-reproducing Antennaria species using a novel target enrichment method that employs custom capture probes designed to work across Asteraceae. Both concatenated and coalescent-based analyses of DNA sequence data from hundreds of nuclear loci recovered Antennaria as a monophyletic group except for the long-disputed species, Antennaria linearifolia, which was recovered outside of the genus. Antennaria was further resolved into three distinct, major lineages. Analysis of ancestral state reconstruction of 12 taxonomically important morphological characters elucidated patterns of character evolution throughout the genus. Estimations of ancestral geographic ranges and molecular dating analyses demonstrated the Rocky Mountain region, including the Vancouverian Province, as the center of origin for the genus Antennaria, around 5.8 MYA. Subsequent dispersals of Antennaria into the Arctic and Appalachian provinces, Canadian provinces, and Eurasia took place roughly 3.2 MYA, 2.4 MYA, and 1.6 MYA, respectively. Biogeographical stochastic mapping indicated that 51.4% of biogeographical events were based on within-area speciation. The remaining 48.6% of the events were divided into two types of dispersals: 1) range expansion dispersals (anagenic, 37%), and 2) founder/jump dispersals (cladogenic, 11.6%). Our results provide a framework for future evolutionary studies of Antennaria, including speciation, origin(s) of polyploidy, and agamospermy in the genus. The Erratum for this article can be found in  Systematic Botany 45(3).