Physical barriers to gene flow were once viewed as prerequisites for adaptive evolutionary divergence. However, a growing body of theoretical and empirical work suggests that divergence can proceed within a single population. Here we document genetic structure and spatially-replicated patterns of phenotypic divergence within a bird species endemic to 250 km2 Santa Cruz Island, California, USA. Island scrub-jays (Aphelocoma insularis) in three separate stands of pine habitat had longer, shallower bills than jays in oak habitat, a pattern that mirrors adaptive differences between allopatric populations of the species’ mainland congener. Variation in both bill measurements was heritable, and island scrub-jays mated non-randomly with respect to bill morphology. The population was not panmictic; instead, we found a continuous pattern of isolation by distance across the east-west axis of the island, as well as a subtle genetic discontinuity across the boundary between the largest pine stand and adjacent oak habitat. The ecological factors that appear to have facilitated adaptive differentiation at such a fine scale—environmental heterogeneity and localized dispersal—are ubiquitous in nature. These findings support recent arguments that microgeographic patterns of adaptive divergence may be more common than currently appreciated, even in mobile taxonomic groups like birds.