Sea anemones (Phylum Cnidaria; Class Anthozoa, Order Actiniaria) exhibit a diversity of developmental patterns that include cloning by fission. Because natural histories of clonal and aclonal sea anemones are quite different, the gain and loss of fission is an important feature of actiniarian lineages. We have used mitochondrial DNA and nuclear intron DNA phylogenies to investigate the evolution of longitudinal fission in sixteen species in the genus Anthopleura, and reconstructed an aclonal ancestor that has given rise at least four times to clonal descendents. For A. elegantissima from the northeastern Pacific Ocean, a transition to clonality by fission was associated with an up-shore habitat shift, supporting prior hypotheses that clonal growth is an adaptation to the upper shore. Fission in Actiniaria likely precedes its advent in Anthopleura, and its repeated loss and gain is perplexing. Field studies of the acontiate sea anemone Aiptasia californica provided insight to the mechanisms that regulate fission: subtidal Aiptasia responded to experimentally destabilized substrata by increasing rates of pedal laceration. We put forth a general hypothesis for actiniarian fission in which sustained tissue stretch (a consequence of substratum instability or intrinsic behavior) induces tissue degradation, which in turn induces regeneration. The gain and loss of fission in Anthopleura lineages may only require the gain and loss of some form of stretching behavior. In this view, tissue stretch initiates a cascade of developmental events without requiring complex gene regulatory linkages.