Presented here is the first characterized remipede toxin, Xibalbin3-Xt3a (Xt3a), a disulfide-rich peptide derived from the venom of a remipede crustacean Xibalanus tulumensis. In contrast to the majority of single domain neurotoxins present in animal venoms, Xt3a has an unusual tandem repeat architecture, consisting of two inhibitor cystine knot (ICK) motifs. This is only the third double-ICK toxin characterized, with the previous two examples found in spiders. In spiders, the tandem repeat architecture leads to high receptor avidity, via a bivalent mode of action. Here, we present the high-resolution solution structure of Xt3a using multidimensional NMR spectroscopy – the first remipede toxin structure reported to date. The structure reveals a novel domain arrangement with an extended and disordered N-terminal tail. Sequence analysis reveals the individual domains of the peptide have sequence similarity to a family of scorpion toxins known to target the ryanodine receptor (RyR); the intracellular calcium release channel that regulates excitation-contraction coupling in muscle cells. Single-channel electrophysiology confirms Xt3a as a potent RyR modulator. The peptide has a complex mode-of-action, which includes high-affinity activation via a sub-conductance state and low affinity channel inhibition. The peptide is further found to have a persistent and long-lasting effect, analogous to the previous tandem repeat toxins described from spiders. These results reveal convergent evolution of RyR targeting peptides in remipede and scorpion venoms, while the tandem repeat architecture of the ICK motif is the first evidence of this evolutionary innovation outside of spiders.