Whether large-scale variation in lineage diversification rates can be predicted by species properties at the population level is a key unresolved question at the interface between micro- and macroevolution. All else being equal, species with biological attributes that confer metapopulation stability should persist more often at timescales relevant to speciation and so give rise to new (incipient) forms that share these biological traits. Here, we develop a framework for testing the relationship between metapopulation properties related to persistence and phylogenetic speciation rates. We illustrate this conceptual approach by applying it to a long-term dataset on demersal fish communities from the North American continental shelf region. We find that one index of metapopulation persistence has phylogenetic signal, suggesting that traits are connected with range-wide demographic patterns. However, there is no relationship between demographic properties and speciation rate. These findings suggest a decoupling between ecological dynamics at decadal timescales and million-year clade dynamics, raising questions about the extent to which population-level processes observable over ecological timescales can be extrapolated to infer biodiversity dynamics more generally.