Aim: Uniform spatial population distributions are predicted to result in lower among-population genetic differentiation and higher within-population genetic diversity than naturally patchy distributions, but there have been surprisingly few attempts to isolate this effect from confounding factors. We studied the widespread wind-pollinated shrub Allocasuarina humilis that is common in a geologically-stable landscape characterised by long-term population persistence to test the influence of semi-continuous versus patchy population distributions on genetic patterns. We also investigated whether A. humilis shows the high population connectedness and genetic diversity typically associated with wind pollination, a relatively uncommon and little-studied syndrome in this landscape. Location: Heath-shrublands (‘heath’) and forests of south-western Australia. Methods: Populations were sampled from heath and forest regions, which respectively exhibited semi-continuous and patchy population distributions. Genetic structure and diversity were assessed for 27 populations using eight nuclear microsatellite markers and three chloroplast regions. Phylogeographic history was examined using Bayesian phylogeny reconstruction, parsimony analysis and tests of expansion. Results: High haplotype diversity is consistent with long-term population persistence across most of the species’ range. Nuclear markers showed low overall population differentiation and no geographical structure over ~900 km, reflecting extensive pollen dispersal. For both marker types, patchily-distributed forest populations were substantially more differentiated with significantly lower within-population diversity than semi-continuous heath populations. Phylogeographic analysis revealed evidence for earlier colonization of heath than forest and recent expansion into wetter forests, consistent with progressive long-term climatic drying. Main conclusions: High population connectedness and genetic diversity probably resulted from wind pollination in combination with dioecy and long life span. Patchy population distributions appear to have influenced genetic structure and diversity through lower pollen and seed dispersal, lower effective population sizes and greater genetic drift. Our approach illustrates the value of minimising confounding variables by testing the effect of a variable ecological trait within a single species.