Ion‐microprobe ²⁰⁶Pb/²³⁸U geochronology and trace element geochemistry of the unpolished rims and sectioned interiors of zircons from Yellowstone caldera's oldest post‐caldera lavas provide insight into the magmatic system during the prelude and aftermath of the caldera‐forming Lava Creek supereruption. The post‐caldera lavas compose the Upper Basin Member of the Plateau Rhyolite and fall into two groups based on zircon crystallization age: early lavas with zircon ages between ~750 and 550 ka and late lavas with zircon ages between ~350 and 250 ka. Zircons from the early‐erupted East Biscuit Basin flow yield U‐Pb dates and trace element compositions, which when considered with the Pb isotopic compositions of their coexisting feldspars and pyroxenes, point to an isotopically distinct parental melt present during crystallization of the Lava Creek magma but untapped by the supereruption. Distinct zircon crystallization ages and Pb‐isotope compositions of major minerals between the early and late Upper Basin Member groups suggest contrasting sources in the magma reservoir. As proxies for melt evolution, the zircons indicate that Yellowstone's post‐caldera rhyolites became more evolved between mid‐ to late‐Pleistocene time, during the same interval that melting of hydrothermally altered wall rock and recharge by new silicic magmas changed in their relative roles. The results from this study indicate that discrete and ephemeral bodies of silicic magma, at times within a mush dominated reservoir and including during the prelude to the Lava Creek eruption, have characterized Yellowstone's subvolcanic reservoir.