What genomic innovations supported the emergence of multicellular animals, over 600 million years ago, remains one of the most fundamental questions in evolutionary biology. Increasing evidence suggests that the elaboration of the regulatory mechanisms controlling gene expression, rather than gene innovation, underlies this transition. Since transcriptional regulation is largely achieved through the binding of specific transcription factors to specific cis-regulatory DNA, understanding the early evolution of these master orchestrators is key to retracing the origin of animals (metazoans). Basic leucine zipper (bZIP) transcription factors constitute one of the most ancient and conserved families of transcriptional regulators. They play a pivotal role in multiple pathways that regulate cell decisions and behaviours in all kingdoms of life. Here, we explore the early evolution and putative roles of bZIPs in a representative of one of the oldest surviving animal groups, the marine sponge Amphimedon queenslandica. Phylogenetic analyses identify 17 bZIPs in Amphimedon, originating from a repertoire of 7 and 12 bZIPs in the metazoan and holozoan ancestor, respectively. As expected for regulatory molecules, most bZIPs display high temporal specificity, cell-type specific localization and are dynamically expressed throughout Amphimedon development. Specific sponge bZIPs appear to be involved in a variety of contexts, including cell fate decisions, circadian regulation and response to pathogens. Integrating these observations with ongoing ChIP-Seq experiments, we infer that many of the roles bZIPs play in bilaterians have a more ancient origin and were present in the last common ancestor of all contemporary animals.