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The defensive use of cone snail venom is hypothesised to have first arisen in ancestral worm-hunting snails and later repurposed in a compartmentalised venom duct to facilitate the dietary shift to molluscivory and piscivory. Consistent with its placement in a basal lineage, we demonstrate that the <i>C. distans</i> venom gland lacked distinct compartmentalisation. Transcriptomics revealed <i>C. distans</i> expressed a wide range of structural classes, with inhibitory cysteine knot (ICK)-containing peptides dominating. To better understand the evolution of the venom gland compartmentalisation, we compared <i>C. distans</i> to <i>C. planorbis</i>, the earliest diverging species from which a defence-evoked venom has been obtained, and fish-hunting <i>C. geographus</i> from the <i>Gastridium</i> subgenus that injects distinct defensive and predatory venoms. These comparisons support the hypothesis that venom gland compartmentalisation arose in worm-hunting species and enabled repurposing of venom peptides to facilitate the dietary shift from vermivory to molluscivory and piscivory in more recently diverged cone snail lineages.