Relatively large new samples of the rare plesiadapid mammal Chiromyoides are reported from upper Paleocene rocks exposed along the eastern flank of the Rock Springs Uplift and the adjacent Washakie Basin in southwestern Wyoming. These specimens form the basis for the new upper Tiffanian species Chiromyoides kesiwah and enhance our knowledge of the anatomy of early Clarkforkian C. gingerichi. Multiple previously unreported or unrecognized specimens of Chiromyoides are also described from upper Paleocene faunas in Texas, Colorado, and Wyoming, enabling a new phylogenetic analysis of all known species of Chiromyoides and selected other plesiadapids and outgroup taxa. The phylogeny of Chiromyoides appears to have been more complicated than previously described, partly because the genus was more speciose than previously appreciated. European C. campanicus and C. mauberti are sister taxa that are deeply nested within an otherwise North American radiation of Chiromyoides, suggesting that Chiromyoides originated in North America before dispersing to Europe in the latter part of the Tiffanian. Most of the derived anatomical features that distinguish Chiromyoides from closely related plesiadapids indicate that it was yet another occupant of the lucrative ‘mammalian woodpecker’ niche, alongside the extant Malagasy lemur Daubentonia, the extant phalangeroid marsupial Dactylopsila, early Cenozoic placental Apatemyidae, and possibly the middle Cenozoic metatherian Yalkaparidon.