Our understanding of population history in deep time has been assisted by fitting admixture graphs ('AGs') to data: models that specify the ordering of population splits and mixtures, which along with the amount of genetic drift on each lineage and the proportions of mixture, is the only information needed to predict the patterns of allele frequency correlation among populations. Not needing to specify population size changes, split times, or whether admixture events were sudden or drawn out simplifies the space of models that need to be searched. However, the space of possible AGs relating populations is vast and cannot be sampled fully, and thus most published studies have identified fitting AGs through a manual process driven by prior hypotheses, leaving the vast majority of alternative models unexplored. Here, we develop a method for systematically searching the space of all AGs that can incorporate non-genetic information in the form of topology constraints. We implement this findGraphs tool within a software package, ADMIXTOOLS 2, which is a reimplementation of the ADMIXTOOLS software with new features and large performance gains. We apply this methodology to identify alternative models to AGs that played key roles in eight published studies and find that graphs modeling more than six populations and two or three admixture events are often not unique, with many alternative models fitting nominally or significantly better than the published one. Our results suggest that strong claims about population history from AGs should only be made when all well-fitting and temporally plausible models share common topological features. Our re-evaluation of published data also provides insight into the population histories of humans, dogs, and horses, identifying features that are stable across the models we explored, as well as scenarios of populations relationships that differ in important ways from models that have been highlighted in the literature, that fit the allele frequency correlation data, and that are not obviously wrong.