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Although behaviors may remain highly conserved through evolutionary time, the ecological functions they serve can undergo surprising transformations. We used phylogenetic, correlational, and experimental evidence to show how a > 150-million year-old behavior, which originally evolved to facilitate migration, has been co-opted for flash flood escape in two distantly related giant water bug species (Hemiptera: Belostomatidae). Using behavioral experiments with simulated rainfall, we showed that species from flash-flooding as well as non-flash-flooding environments are capable of rainfall response behavior (RRB), the ability to use rainfall as a cue to abandon an aquatic habitat. The results suggest that, in addition to allowing individuals to escape flash floods, RRB is the proximate mechanism generating a well-established ecological pattern: The correlation between rainfall and migration to seasonal breeding habitats that has been documented in 13 species throughout the family. Placing RRB in phylogenetic context reveals that for several taxa the behavior is an exaptation (a trait evolved for one function but later co-opted for another) for escaping flash floods. For Lethocerus medius, rainfall response behavior is an addition exaptation because the behavior is used to initiate migration to seasonal rain pools ( ancestral function) as well as for flash flood escape (co-opted function). In the distantly related Abedus herberti, rainfall response behavior is a transfer exaptation because it has been co-opted exclusively for flash flood escape and the ancestral function has been lost. These findings emphasize that a phylogenetic framework is needed to fully understand the origins and ecological significance of behaviors.