Symbiotic relationships are ubiquitous across nature and play key roles in the maintenance of biodiversity and ecosystem function. The Myzostomida are an enigmatic clade of marine annelids that live as obligate symbionts on or inside their predominantly echinoderm hosts. Species of myzostomid have diverse morphologies and lifestyles, ranging from cyst and gall forming, to parasitic host eating, and free-living ectocommensalism. Largely described from shallow tropical waters, there is currently limited information on myzostomids from the deep sea. Here we describe, using integrated morphological and molecular data, the first genus and two species of myzostomid from the abyssal seafloor, found living ectocommensally on porcellanasterid starfish from 3490 to 4362 m deep in the central and North Pacific Ocean. Molecular phylogenetic analyses using both nuclear (18S rRNA, H3) and mitochondrial (COI, 16S rRNA) markers recovered Myrmekimyzostomumgen. nov. as monophyletic, and the sole commensal genus in a clade of parasitic species associated with asteroids and ophiuroids. Trait-mapping across the phylogeny suggests the ancestral myzostomid form likely lived ectocommensally on stalked crinoids, with parasitism emerging multiple times in their evolutionary history. These new taxa underline the substantial ecological and evolutionary novelty that can be found in the deep sea. Zoobank: urn:lsid:zoobank.org:pub:332B8B95-F390-4D9F-B1FE-E9E4D433E24C.