Background: Temnothorax (Formicidae: Myrmicinae) is a diverse genus of ants found in a broad spectrum of ecosystems across the northern hemisphere. These diminutive ants have long served as models for social insect behavior, leading to discoveries about social learning and inspiring hypotheses about the process of speciation and the evolution of social parasitism. This genus is highly morphologically and behaviorally diverse, and this has caused a great deal of taxonomic confusion in recent years. Past efforts to estimate the phylogeny of this genus have been limited in taxonomic scope, leaving the broader evolutionary patterns in Temnothorax unclear. To establish the monophyly of Temnothorax, resolve the evolutionary relationships, and investigate trends in the evolution of key traits, I generated, assembled, and analyzed two molecular datasets: a traditional multi-locus Sanger sequencing dataset, and an ultra-conserved element (UCE) dataset. Using maximum likelihood, Bayesian and summary-coalescent based approaches, I analyzed 22 data subsets consisting of 103 ingroup taxa and a maximum of 1.8 million base pairs in 2,485 loci. Results: The results of this study suggest an origin of Temnothorax at the Eocene-Oligocene transition, concerted transitions to arboreality in the Oligocene in several clades, coinciding with ancient global cooling, and several convergent origins of social parasitism in the Pliocene. As with other Holarctic taxa, Temnothorax has a history of migration across Beringia during the Miocene. Conclusions: Temnothorax is corroborated as a natural group, and the notion that many of the historical subgeneric and species group concepts are artificial is reinforced. The strict form of Emery's Rule, in which a socially parasitic species is sister to its host species, is not well supported in Temnothorax.