<title>Abstract</title>Among over 20,000 species of Annelida, only two branching species with a highly modified body-pattern are known until now: the Syllidae <italic>Syllis ramosa</italic> McIntosh, 1879, and <italic>Ramisyllis multicaudata</italic> Glasby et al. (Zoological Journal of the Linnean Society, 164, 481–497, 2012). Both have unusual ramified bodies with one head and multiple branches and live inside the canals of host sponges. Using an integrative approach (combining morphology, internal anatomy, ecology, phylogeny, genetic divergence, and the complete mitochondrial genome), we describe a new branching species from Japan, <italic>Ramisyllis kingghidorahi</italic> n. sp., inhabiting an undescribed species of <italic>Petrosia</italic> (Porifera: Demospongiae) from shallow waters. We compare the new species with its closest relative, <italic>R. multicaudata</italic>; emend the diagnosis of <italic>Ramisyllis</italic>; and discuss previous reports of <italic>S. ramosa</italic>. This study suggests a much higher diversity of branching syllids than currently known. Finally, we discuss possible explanations for the feeding behaviour in the new species in relation to its highly ciliated wall of the digestive tubes (especially at the distal branches and anus), and provide a hypothesis for the evolution of branching body patterns as the result of an adaptation to the host sponge labyrinthic canal system.