We present new sanidine ⁴⁰Ar/³⁹Ar ages and paleomagnetic data for pre- and post-caldera rhyolites from the second volcanic cycle of the Yellowstone Plateau volcanic field, which culminated in the caldera-forming eruption of the Mesa Falls Tuff at ca. 1.3 Ma. These data allow for a detailed reconstruction of the eruptive history of the second volcanic cycle and provide new insights into the petrogenesis of rhyolite domes and flows erupted during this time period. ⁴⁰Ar/³⁹Ar age data for the biotite-bearing Bishop Mountain flow demonstrate that it erupted approximately 150 kyr prior to the Mesa Falls Tuff. Integrating ⁴⁰Ar/³⁹Ar ages and paleomagnetic data for the post-caldera Island Park rhyolite domes suggests that these five crystal-rich rhyolites erupted over a centuries-long time interval at 1.2905 ± 0.0020 Ma (2σ). The biotite-bearing Moonshine Mountain rhyolite dome was originally thought to be the downfaulted vent dome for the pre-caldera Bishop Mountain flow due to their similar petrographic and oxygen isotope characteristics, but new ⁴⁰Ar/³⁹Ar dating suggest that it erupted near contemporaneously with the Island Park rhyolite domes at 1.2931 ± 0.0018 Ma (2σ) and is a post-caldera eruption. Despite their similar eruption ages, the Island Park rhyolite domes and the Moonshine Mountain dome are chemically and petrographically distinct and are not derived from the same source. Integrating these new data with field relations and existing geochemical data, we present a petrogenetic model for the formation of the post-Mesa Falls Tuff rhyolites. Renewed influx of basaltic and/or silicic recharge magma into the crust at 1.2905 ± 0.0020 Ma led to [1] the formation of the Island Park rhyolite domes from the source region that earlier produced the Mesa Falls Tuff and [2] the formation of Moonshine Mountain dome from the source region that earlier produced the biotite-bearing Bishop Mountain flow. These magmas were stored in the crust for less than a few thousand years before being erupted contemporaneously along a 30 km long, structurally controlled vent zone related to extracaldera Basin and Range faults. These data highlight the rapidity with which magma can be generated and erupted over large distances at Yellowstone.