Sponges (Porifera) form symbiotic relationships with specific bacteria while relying on free-living bacteria for nutrition. To explore how sponges discriminate symbiotic from food bacteria, we present juveniles of the marine demosponge Amphimedon queenslandica with bacterial enrichments from conspecifics and from another species of sponge, and observe their transcriptional response. Compared with non-symbionts, symbionts induce a much more pronounced transcriptional response within just 2 hours. Specifically, the sponge mounts a striking and rapid innate immune response to its bacterial symbionts, but not to non-symbionts. This includes the upregulation of a distinct suite of pattern recognition receptors (e.g., scavenger receptor cysteine-rich superfamily and immunoglobulins), innate immune pathways (e.g., Toll signaling and janus kinase-signal transducer and activator of transcription), and conserved immune transcription factors (e.g., nuclear factor kappa-light-chain-enhancer of activated B cells and interferon regulatory factor) within 2 hours. At this time, we also observe the sponge cells interact with symbionts differently from non-symbionts, with the former being transferred more rapidly from choanocytes into mobile archaeocytes. Given the phylogenetic position of sponges as sister to all other animals, our findings suggest the involvement of innate immunity in the interactions with bacterial symbionts is deeply rooted in the origin and early evolution of metazoans.