Insect wings undergo large, passive deformations during flight, which are controlled primarily by the architecture and material properties of the wing. The pattern of supporting veins in wings varies widely among insect orders and families, but the functional significance of these phylogenetic trends remains unclear, and the degree to which stiffness varies within an individual wing is unknown. To assess the relationship between wing venation and stiffness, I measured flexural stiffness and quantified venation pattern in 16 insect species from 6 orders. These measurements reveal that spanwise stiffness scales strongly with the cube of wing span, whereas chordwise stiffness scales with the square of chord length. In addition, spanwise stiffness is 1 to 2 orders of magnitude greater than chordwise stiffness. Independent contrasts of flexural stiffness and wing venation characters are uncorrelated, but a finite element model of a wing suggests that the leading edge veins play an important role in generating the spanwise-chordwise anisotropy measured in real wings. To further understand how stiffness varies within a wing, I measured spatial patterns of flexural stiffness in the wings of hawkmoths (Manduca sexta) and dragonflies (Aeshna multicolor). In both species, flexural stiffness declines exponentially from wing base to tip and from the leading to the trailing edge. Finite element models based on the wings of M. sexta demonstrate that this sharp decline in stiffness preserves rigidity in proximal regions of the wing, while transferring bending to the edges, where aerodynamic force production is most sensitive to subtle shape changes.