Although an implicit assumption of speciation biology is that population differentiation is an important stage of evolutionary diversification, its true significance remains largely untested. If population differentiation within a species is related to its speciation rate over evolutionary time, the causes of differentiation could also be driving dynamics of organismal diversity across time and space. Alternatively, geographic variants might be short-lived entities with rates of formation that are unlinked to speciation rates, in which case the causes of differentiation would have only ephemeral impacts. Combining population genetics datasets including 17,746 individuals from 176 New World bird species with speciation rates estimated from phylogenetic data, we show that the population differentiation rates within species predict their speciation rates over long timescales. Although relatively little variance in speciation rate is explained by population differentiation rate, the relationship between the two is robust to diverse strategies of sampling and analyzing both population-level and species-level datasets. Population differentiation occurs at least three to five times faster than speciation, suggesting that most populations are ephemeral. Population differentiation and speciation rates are more tightly linked in tropical species than temperate species, consistent with a history of more stable diversification dynamics through time in the Tropics. Overall, our results suggest investigations into the processes responsible for population differentiation can reveal factors that contribute to broad-scale patterns of diversity.