Viral envelope glycoproteins mediate membrane fusion, dictate host range and facilitate virus immune evasion. The proteins’ important roles paired with the fast evolutionary rate of viruses lead to rapid accumulation of changes in their sequences, hindering homology detection over deep evolutionary time. Recent AI-based methods such as AlphaFold and ESMfold have enabled fast and accurate prediction of protein structures from sequence alone. We leverage these structural prediction methods at scale to infer homology and the evolutionary histories of viral glycoproteins by pairing both sequence but also structural similarity between them. Applied to the large Flaviviridae virus family, this approach allows us to uncover the wide diversity of entry mechanisms they utilise and associate these with the viruses’ host ecology. Finally, our work establishes the foundations of protein structure-based phylogenetics which can help us investigate the yet unexplored relation between sequence and structural protein evolution.