Bonebeds are vertebrate bioclast concentrations in beds that are local to basinal in extent. The middle Miocene Sharktooth Hill bonebed in the southeastern San Joaquin Basin of California is among the largest of such deposits, exposed over 15 km and containing a rich assemblage of marine vertebrates, with a mean density of ~200 specimens/m2. It ranks among the most widespread and richest bonebeds known, yet its genesis is poorly understood. Hypotheses for its origin and formation include mass death from shark predation, volcanic or red tide poisoning, accumulation from a calving ground for marine mammals, and condensed accumulation over a long period of time. Based on multiple kinds of evidence, we conclude that the bonebed formed over a protracted time interval of little to no net clastic sedimentation, coincident with a significant transgressive-regressive cycle between 16 and 15 Ma ago, during the middle Miocene Climatic Optimum (MMCO). Geochronological constraints bracket the duration of bonebed formation to no longer than 700 ka, indicating that time averaging is a critical consideration for paleoecological analyses of North Pacific Ocean biotic richness during the MMCO.