Discovering the functions of uncharacterised genes is a major challenge in modern biology, but it is rarely undertaken within a robust evolutionary framework. EcKinases, a largely arthropod-specific family of small-molecule kinases, are implicated in the regulation of ecdysteroids in reproduction and development, but some lines of evidence suggest they detoxify phytoecdysteroids in the diets of crop pest insects, and they may act as a novel, non-canonical family of Phase II detoxification enzymes. However, this family is broadly uncharacterised, and its evolutionary history has not been studied. To address this, we have manually annotated EcKinases in the genomes of over 60 species of arthropods and used Bayesian phylogenetic methodologies to reconstruct their evolution phylum-wide. EcKinases were found in the genomes of hexapods and crustaceans, but not chelicerates and myriapods. Gene content per genome ranges from 12 (in many bee species) to 104 (in the German cockroach). Some taxa, like bees, exhibit remarkable stability in gene content, while others, like the Drosophila genus and related Dipteran taxa, have experienced rapid gene gain and loss. Polyphagous Lepidopteran species have undergone independent gene blooms in clades predicted to be ecdysteroid kinases, suggesting they may play a role in phytochemical detoxification. Various single-copy clades are highly conserved in insects, pointing to roles in biological processes fundamental to this taxon. These results and ongoing work are providing an informative framework for characterising EcKinase gene function across the arthropod phylum.