Marine cone snails have attracted researchers from all disciplines but early life stages have received limited attention due to difficulties accessing or rearing juvenile specimens. Here, we document the culture of Conus magus from eggs through metamorphosis to reveal dramatic shifts in predatory feeding behaviour between post-metamorphic juveniles and adult specimens. Adult C. magus capture fish using a set of paralytic venom peptides combined with a hooked radular tooth used to tether envenomed fish. In contrast, early juveniles feed exclusively on polychaete worms using a unique “sting-and-stalk” foraging behaviour facilitated by short, unbarbed radular teeth and a distinct venom repertoire that induces hypoactivity in prey. Matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF-MS) on a timsTOF fleX MALDI-2 MS (Bruker) revealed that juvenile and adult VG proteomes were dominated by distinct suites of peptides < 6 kDa, with masses > 4 kDa restricted to the adult VG. HPLC coupled to ZenoTOF 7600 MS (SIEX) revealed few common masses and confirmed the juvenile VG proteome was largely dominated by peptides falling into the 1–2 kDa mass range, while the adult VG proteome contained a large proportion of 4–6 kDa peptides. To evaluate the pharmacological potential of novel sequences identified, we used sequence homology and AlphaFold to identify likely bioactive peptides to synthesise for evaluation across selected high throughput screens. Our results demonstrate how coordinated morphological, behavioural and molecular changes facilitate the shift from worm- to fish-hunting in C. magus and showcase juvenile cone snails as a rich and unexplored source of novel venom peptides for biodiscovery.