Habitat selection that maximizes both larval settlement success and subsequent juvenile and adult performance is a fundamental challenge for marine benthic organisms with complex life histories (e.g., planktonic larvae). For benthic herbivores, chemical cues from macroalgae can strongly influence both larval settlement/metamorphosis and subsequent performance. We compared the effects of chemical cues from host algae on different life history stages of the “arboreal” sea urchin Holopneustes purpurascens. In sublittoral habitats near Sydney, Australia, H. purpurascens occurred primarily on two algal hosts: red alga (Delisea pulchra) and kelp (Ecklonia radiata). Urchins on E. radiata were significantly larger than those on D. pulchra, but no recruits occurred on E. radiata. In experiments, larvae rapidly metamorphosed in the presence of D. pulchra, but metamorphosis was delayed or nonexistent in the presence of E. radiata. D. pulchra produces a polar chemical inducer of metamorphosis not found in E. radiata. In contrast to larval metamorphosis, feeding and performance of juvenile and adult urchins were considerably worse on D. pulchra than on E. radiata. Feeding experiments confirmed that nonpolar metabolites (halogenated furanones) in D. pulchra deter feeding. Adding natural concentrations of the most abundant furanone to otherwise palatable diets completely inhibited feeding. Urchins fed D. pulchra had reduced survival, growth, and reproduction compared to those fed E. radiata. H. purpurascens did not thrive on the alga on which they preferentially settled; therefore, postrecruitment movement from D. pulchra to E. radiata was crucial to fitness. Urchins in D. pulchra beds moved between plants at night and preferred E. radiata in habitat preference experiments. Movement was constrained by diurnal predators, particularly damselfish Parma microlepis. When H. purpurascens was removed from their algal hosts during the day (but not at night), P. microlepis “clipped” their spines and tube feet. Removal of 10% of an urchin's spines and tube feet was fatal. H. purpurascens recruits onto a host that does not support persistence of the benthic phase and then shifts host plants, incurring a predation risk. Though chemically mediated, ontogenetic shifts in host plant use are known for insect herbivores, this is the first known example in a marine herbivore.