We evaluated the fossil record of extinct and extant woodrats, and generated a comprehensive phylogenetic hypothesis of woodrat origins and relationships based on these data. The galushamyinin cricetines are redefined and reclassified as a subtribe of the Neotomini, including Repomys, Miotomodon, Galushamys, Nelsonia, and a new extinct genus with two new species. The geographic distribution of Nelsonia, restricted to montane coniferous forests of western Mexico, suggests that this subtribe was mostly confined to western coniferous ecosystems or similar ecosystems at lower elevation during glacial advances. A second subtribe of the Neotomini includes a new archaic genus and species, Neotoma, Hodomys, and Xenomys. Lindsaymys, a possible neotominin from the late Clarendonian (late Miocene) of California, demonstrates an occlusal morphology consistent with ancestry for the Neotomini, but the presence of a fourth root on M1 is problematic and may preclude the known populations from filling that role. Molars identified as Neotoma sp. from the Hemphillian (latest Miocene or early Pliocene) Rancho el Ocote assemblage of Guanajuato, Mexico, may represent the earliest Xenomys. Extant Neotoma species with a bilobed m3 appear to have originated subsequent to about 2.0 Ma, whereas Hodomys alleni and Xenomys nelsoni likely originated earlier from one or more extinct ancestors with an S-shaped m3.