Structural colour is an optical phenomenon resulting from light interacting with nanostructured materials. Although structural colour is widespread in the tree of life, the underlying genetics and genomics are not well understood. Here we collected and sequenced a set of 87 structurally coloured bacterial isolates, and 30 related strains lacking SC. Optical analysis of colonies indicated that diverse bacteria from at least two different phyla (Bacteroidetes and Proteobacteria) can create two dimensional packing capable of producing SC. Pan-genome-wide association approaches were used to identify genes associated with structural colour. The biosynthesis of uroporphyrin and pterins, as well as carbohydrate utilisation and metabolism, were found to be involved. Using this information, we constructed a classifier to predict structural colour directly from bacterial genome sequences, validated it by scoring 100 strains that were not involved in creating the structural colour classifier, and predicted that photonic structures are widely distributed within Gram-negative bacteria. Analysis of over 13 thousand assembled metagenomes predicted that SC is nearly absent from most habitats associated with multicellular organisms except macroalgae and is abundant in marine waters and surface/air interfaces. This work provides the first large-scale ecogenomics view of structural colour in bacteria and identifies microbial pathways and evolutionary relationships that underlie this optical phenomenon.