Interactions of membrane proteins with lipid molecules are central to their stability and function. We have used multiscale molecular dynamics simulations to determine the extent to which interactions with lipids are conserved across the aquaporin (Aqp) family of membrane proteins. Simulation-based assessment of the lipid interactions made by Aqps when embedded within a simple phospholipid bilayer agrees well with the protein-lipid contacts determined by electron diffraction from 2D crystals. Extending this simulation-based analysis to all Aqps of known structure reveals a degree of conservation of such interactions across the Aqp structural proteome. Despite similarities in the binding orientations and interactions of the lipids, there do not appear to be distinct, high-specificity lipid binding sites on the surface of Aqps. Rather Aqps exhibit a more broadly conserved protein/lipid interface, suggestive of interchange between annular and bulk lipids, instead of a fixed annular "shell" of lipids.