Flight plays a central role in dragonfly feeding, reproduction, predator avoidance, and dispersal. Some dragonflies, “perchers”, engage in short distance flights or territorial patrols from perching locations. Others, “fliers”, fly for longer periods of time, with some dragonflies, such as Anax or Pantala, migrating great distances. In general, fliers and perchers differ in their morphometric features and taxonomic affinities and may have adapted different wing venation patterns to meet their characteristic flight requirements. We might expect perchers, for example, to possess vein patterns that increase rigidity in regions affecting flight stability and allow for elasticity and flexibility in regions that are important for maneuverability. Vein patterns of fliers, on the other hand, should allow for faster, longer distance flight, in less confined areas. Some, especially fliers depending on gliding during long flights, have expanded hindwing anal areas and concomitant modifications of anal veins. To determine whether there are consistent differences between the wing characteristics of percher and flier dragonflies, we measured the lengths of 50 wing veins and 42 vein ratios. Three regions of the wing were found to differ significantly in perchers and fliers: the anal vein region, the discoidal field and the nodus region. Mechanical effects of these differences are as yet unknown but should be amenable to testing. We reconstructed ancestral vein lengths to explore ancestral flight behavior. Flier-style behaviour is likely the ancestral condition in Anisoptera, with perching behaviour evolving independently several times.