The processes that give rise to species richness gradients are not well understood, but may be linked to resource-based limits on the number of species a region can support. Ecological limits placed on regional species richness should also affect population demography, suggesting that these processes could also generate genetic diversity gradients. If true, we might better understand how broad-scale biodiversity patterns are formed by identifying the common causes of genetic diversity and species richness. We develop a hypothetical framework based on the consequences of regional variation in ecological limits set by resource availability and heterogeneity to simultaneously explain spatial patterns of species richness and neutral genetic diversity. Repurposing raw genotypic data spanning 38 mammal species sampled across 801 sites in North America, we show that estimates of genome-wide genetic diversity and species richness share spatial structure. Notably, species richness hotspots tend to harbor lower levels of within-species genetic variation. A structural equation model encompassing eco-evolutionary processes related to resource availability, habitat heterogeneity, and contemporary human disturbance supports the spatial patterns we detect. These results suggest broad-scale patterns of species richness and genetic diversity could both partly be caused by intraspecific demographic and evolutionary processes acting simultaneously across species.