Phylum Cnidaria (jellyfish, corals, hydroids and sea anemones), an early divergent eumetazoan lineage, is characterised by a lack of an adaptive immune system and hence must rely on the capacity of the innate immune system to cope with selection pressure associated with rapidly-evolving microbes. Interrogation of early divergent lineages may provide us with insights into the evolution and origin of eumetazoan gene sets. Therefore, cnidarians present an excellent avenue for research investigating both conserved and novel innate immune genes in eumetazoans. Here we report the first comprehensive and comparative study on the cnidarian innate immune system, across 13 transcriptomes from nine actiniarian species, to identify the origins, expansions and contractions of highly-conserved candidate gene families and novel innate immune genes. We characterised five candidate gene families; single copies of TLR, MyD88 and NF-κB were found in most species, and several copies of IL-1R and NLR were found in all. A subset of NLRs possessed multiple transmembrane domains, which have so far only been identified in two cnidarian species, suggesting that membrane-bound NLRs may be a uniquely cnidarian innovation. Multiple novel immune genes were also identified with domain architectures including the Toll/interleukin-1 receptor (TIR) homology domain, which is well-documented as functioning in protein-protein interactions and signal transduction in immune pathways. We hypothesise that these genes may interact as novel proteins in immune pathways. Overall, these results provide an insight into the evolution of the innate immune system and show that cnidarians have a diverse repertoire of conserved and novel innate immune genes.