Marine invertebrates with pelagobenthic life cycles have a morphologically distinct planktonic larval form that settles and metamorphoses into a benthic reproductive adult. Settlement and metamorphosis is initiated by environmental cues, which activate internal signaling pathways that lead to cellular and body plan changes. In the demosponge Amphimedon queenslandica, swimming larvae are induced to settle by cues from coralline algae, which activate several conserved signaling pathways, including Delta/Notch, WNT, Ca2+, nitric oxide (NO) and MAPK pathways. Using specific agonists and antagonists, we uncover a complex interplay between Delta/Notch and WNT in controlling the settlement process and the very first steps in the initiation of metamorphosis. Delta/Notch signaling at the larval anterior end is sufficient for initiating settlement and metamorphosis in young competent larvae. This role appears to dissipate as the larva ages. In contrast, WNT plays an inhibitory role, preventing settled larvae from progressing through the first hour of metamorphosis. The role of WNT appears to change later in metamorphosis and is necessary for metamorphosis to progress. These results, combined with those on Ca2+, nitric oxide (NO) and MAPK pathways, suggest that the regulation of A. queenslandica settlement and metamorphosis is remarkably complex and may include pathway convergences and feed-forward mechanisms.