Abstract Vertical gradients in microclimate, resource availability and interspecific interactions are thought to underly stratification patterns in tropical insect communities. However, only a few studies have explored the adaptive significance of vertical space use during early population divergence. We analysed flight-height variation across speciation events in Heliconius butterflies representing parallel instances of divergence between low and high-altitude populations. We measured flight-height in wild H. erato venu s and H. chestertonii , lowland and mountain specialists respectively, and found that H. chestertonii consistently flies at a lower height. We compared these data with previously published results for H. e. cyrbia and H. himera , the latter of which flies lower and, like H. chestertonii , recently colonised high-altitude, dry forests. We show that these repeated trends largely result from shared patterns of selection across equivalent environments, producing parallel trait-shifts in H. himera and H. chestertonii . Although our results imply a signature of local adaptation, we did not find an association between resource distribution and flight-height in H. e. venus and H. chestertonii . We discuss how this pattern may be explained by variation in forest structure and microclimate. Overall, our findings underscore the importance of behavioural adjustments during early divergence mediated by altitude-shifts.