Alligatorines are a diverse clade of crocodylians whose history spans the entire Cenozoic. They are suited to answer a variety of questions with far‐reaching impacts due to their physiology and preservation potential, and have been the subject of several phylogenetic, biogeographic, and diversity analyses. However, prior phylogenetic analyses had poor resolution and several putative alligatorines have never been included, while other analyses would be more informative and accurate if viewed through the context of evolutionary history. Here, I analyze the phylogenetics, taxonomy, biogeography, ecomorphology, and diversity dynamics of alligatorines. An almost fully resolved phylogenetic hypothesis returns two major clades within Alligatorinae and includes several putative alligatorines not previously analyzed. The clade originated in North America and dispersed to Europe and Asia three to five times via at least three different corridors at high latitudes when climate—and potentially salinity—were favorable, likely including the recently discovered subaerial Lomonosov Ridge. The modern American alligator is a dietary generalist, but evolved from a durophagous specialist, contrary to the intuitive reasoning of the “Law of the Unspecialized”. It was able to do so by entering the generalist niche vacated by basal crocodyloids following their extirpation from mid‐latitude North America. Alligatorine diversity only weakly tracks climate change and does not track the rock record excepting swampy environments. Alligatorine diversity correlates with climate change. Climate change correlates with rocks, though in a more complicated pattern. Some diversity metrics correlate with some aspects of the rock record, but predominantly do not. There is more support for the common‐cause hypothesis than for rock record bias driving apparent alligatorine diversity. Overall, alligator evolution exhibits a pattern of being more diverse taxonomically and morphologically when the climate is warmer, and dispersing during the warmest and wettest of those times.