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Abstract Many insect groups have acquired obligate microbial symbionts, and the resulting associations can have important ecological and evolutionary consequences. A notable example among ants is the species‐rich tribe Camponotini, whose members derive nutritional benefits from a vertically inherited bacterial endosymbiont,Blochmannia. We generate ultraconserved element (UCE) phylogenomic data for 220 ingroup and 5 outgroup taxa to reconstruct a detailed evolutionary history of the Camponotini, including the inference of divergence times and dispersal events. Under multiple modes of analysis, including both concatenation and species‐tree approaches, we recover a well‐supported backbone phylogeny comprising eight lineages: three large genera (Camponotus,Colobopsis,Polyrhachis) and several smaller genera or clusters of genera. Three novel lineages are uncovered that cannot be placed in any existing genus:Lathidrisgen. n., from the mountains of Mesoamerica;Retalimyrmagen. n., from the Indian Himalayas; andUwarigen. n., from eastern Asia. The species in these new genera were described and placed erroneously inCamponotus. The tribe Camponotini is estimated to have a crown origin in the Eocene (median age 38.4 Ma), with successively younger crown ages forColobopsis(22.5 Ma),Camponotus(18.6 Ma) andPolyrhachis(18.5 Ma). We infer an Australasian or Indomalayan origin for the tribe, with multiple dispersal events to the Afrotropics, Palearctic region, and New World. Phylogenetic analysis of selectedBlochmanniagenes from a subset of 97 camponotine taxa yields results that are largely congruent with the ant host phylogeny, at least for well‐supported nodes, but we find evidence thatBlochmanniafrom some old lineages—especiallyLathidris—may have discordant histories, suggesting possible lability of this symbiosis in the early evolution of camponotine ants.