The early–middle Miocene was an important transitional period in the evolution of Earth’s biota and climate that has been poorly understood in North America due to a paucity of continuous, fossil-bearing rock records in this interval for which the ages have been robustly constrained. In the northern Rocky Mountains, United States, one site in particular, known as the Railroad Canyon section, has provided biostratigraphic, magnetostratigraphic, and lithostratigraphic evidence suggesting a late early–middle Miocene age; however, radiometrically calibrated age models have been notoriously lacking. To better constrain the age of the Railroad Canyon section and the abundant fossils preserved therein, we employed moderate- and high-precision U-Pb dating of single zircon crystals from four ash horizons throughout the section. The resulting dates span from 22.65 ± 0.37 Ma to 15.76 ± 0.22 Ma. Using these dates, we developed a radiometrically calibrated age model for the Railroad Canyon section that constrains the age of the section to ca. 22.9–15.2 Ma, ∼5 m.y. older than previous estimates. These results firmly establish that the Railroad Canyon section was deposited during buildup to peak warming of the mid-Miocene climatic optimum. Additionally, these dates provide definitive age estimations for the initiation and cessation of the early Miocene unconformity, a regional unconformity exposed in many intermontane basins across the northern Rocky Mountains, as ca. 21.5 and 21.4 Ma, respectively, in the Railroad Canyon section. This new chronostratigraphic analysis provides an impetus for reassessment of the biochronology of the region, in turn suggesting earlier first appearances of many biostratigraphically important taxa found in the northern Rocky Mountains, Great Plains, and American Northwest.