Ecological community structure ultimately depends on evolution producing community members. To understand how macroevolutionary processes shape communities, we surveyed Anolis lizard assemblages across elevations on Jamaica and Hispaniola, neighboring Caribbean islands similar in environment, but contrasting in evolutionary richness. The impact of diversification on local communities depends on available opportunities for speciation within or between ecologically distinct sub-regions. Where opportunities abound, as in the vast lowlands of both islands, communities converge in species richness and average morphology. But community structures diverge in the highlands. On Jamaica, where limited highland area restricted diversification, communities remain depauperate and consist largely of elevational generalists. In contrast, a unique fauna of high-elevation specialists evolved in the expansive Hispaniolan highlands, augmenting highland richness, and driving islandwide turnover in community composition. Accounting for disparate evolutionary opportunities may illuminate when regional diversity will enhance local diversity and help identify the causes of convergent versus divergent community structure.