UNLABELLED: A fully functional Dicer helicase, present in the modern arthropod, uses energy generated during ATP hydrolysis to power translocation on bound dsRNA, enabling the processive dsRNA cleavage required for efficient antiviral defense. However, modern Dicer orthologs exhibit divergent helicase functions that affect their ability to contribute to antiviral defense, and moreover, mechanisms that couple ATP hydrolysis to Dicer helicase movement on dsRNA remain enigmatic. Here, we used biochemical and structural analyses of ancestrally reconstructed Dicer helicases to map evolution of dsRNA binding affinity, ATP hydrolysis and translocation. We found that loss of affinity for dsRNA occurred early in Dicer evolution, coinciding with a decline in translocation activity, despite preservation of ATP hydrolysis activity, exemplified by the ancient deuterostome Dicer. Ancestral nematode Dicer also exhibited significant decline in ATP hydrolysis and translocation, but studies of antiviral activities in the modern nematode SIGNIFICANCE STATEMENT: Among invertebrates, the contribution of Dicer's helicase to recognition and elimination of viral double-stranded RNA varies from phylum to phylum. At the extreme end of the spectrum, vertebrate Dicers show no helicase activity. On the other end, an arthropod ortholog uses helicase translocation to efficiently move double-stranded RNA into Dicer's cleavage site. The biochemical and structural basis of Dicer's helicase function, as well as the evolutionary events that contribute to a divergence in function, have remained unknown. This study shows how ancient Dicer helicase tightly binds double-stranded RNA and couples ATP hydrolysis to movement along this substrate. In addition, the data reveal how components of this intricate system declined along different clades of animal evolution.