The majority of animal species transition between two morphologically and ecologically distinct body plans: a free-swimming, dispersive larva and a benthic adult. Although this biphasic lifecycle is widely distributed across nearly all metazoan phyla, pointing to an ancient synapomorphy, each lineage is characterized by lineage- and taxon-specific morphological adaptations. This provides an excellent comparative framework for the evolution of novelty in animal body plans. Using developmental transcriptome data from the sponge Amphimedon queenslandica as a foundation for lifecycle evolution, we examined how biphasy is orchestrated on a genomic level. We find that the Amphimedon lifecycle is regulated by distinct suites of larval- and adult-specific genes that complement a core set of highly expressed genes that are shared between larval and adult body plans. Moreover, we find that novel poriferan-specific innovations are enriched in the adult transcriptome, while larval and juvenile stages are characterized by the up-regulation of well-conserved metazoan developmental genes. By extending our analyses to the developmental transcriptomes of five eumetazoan phyla, we show that genes differentially expressed in each taxon are largely characterized by lineage-specific co-expression modules, which are driven by both novel and well-conserved transcription factors. We discuss the implications of these results in the context of larval biology and historical embryological theory to provide a new genomically-informed hypothesis for animal lifecycle evolution.