Cenozoic growth of the Alaska Range created the highest topography in North America, but the space-time pattern and drivers of exhumation are poorly constrained. We analyzed U/Pb and fission-track double dates of detrital zircon and apatite grains from 12 catchments that span a 450 km length of the Alaska Range to illuminate the timing and extent of exhumation during different periods. U/Pb ages indicate a dominant Late Cretaceous to Oligocene plutonic provenance for the detrital grains, with only a small percentage of grains recycled from the Mesozoic and Paleozoic sedimentary cover. Fission-track ages record exhumation during Alaska Range growth and incision and reveal three distinctive patterns. First, initial Oligocene exhumation was focused in the central Alaska Range at ~30 Ma and expanded outward along the entire length of the range until 18 Ma. Oligocene exhumation, coeval with initial Yakutat microplate collision >600 km to the southeast, suggests a far-field response to collision that was localized by the Denali Fault within a weak Mesozoic suture zone. Second, the variable timing of middle to late Miocene exhumation suggests independently evolving histories influenced by local structures. Time-transgressive cooling ages suggest successive rock uplift and erosion of Mounts Foraker (12 Ma) through Denali (6 Ma) as crust was advected through a restraining bend in the Denali Fault and indicate a long-term slip rate ~4 mm/yr. Third, Pliocene exhumation is synchronous (3.7–2.7 Ma) along the length of the Alaska Range but only occurs in high-relief, glacier-covered catchments. Pliocene exhumation may record an acceleration in glacial incision that was coincident with the onset of Northern Hemisphere glaciation.