Comparative population genomics is an ascendant field using genomic comparisons between species to draw inferences about forces regulating genetic variation. Comparative phylogeography, by contrast, focuses on the shared lineage histories of species co-distributed geographically and is decidedly organismal in perspective. Comparative phylogeography is approximately 35 years old, and, by some metrics, is showing signs of reduced growth. Here we contrast the goals and methods of comparative population genomics and comparative phylogeography and argue that comparative phylogeography offers an important perspective on evolutionary history that succeeds in integrating genomics with landscape evolution in ways that complement the suprageographic perspective of comparative population genomics. Focusing primarily on terrestrial vertebrates, we review the history of comparative phylogeography, its milestones and ongoing conceptual innovations, its increasingly global focus and its status as a bridge between landscape genomics and the process of speciation. We also argue that, as a science with a strong “sense of place”, comparative phylogeography offers abundant “place-based” educational opportunities with its focus on geography and natural history, as well as opportunities for collaboration with local communities and indigenous peoples. Although comparative phylogeography does not yet require whole genome sequencing for many of its goals, we conclude that it nonetheless plays an important role in grounding our interpretation of genetic variation in the fundamentals of geography and Earth history.