Conopeptides are a diverse group of recently evolved venom peptides that are used for prey capture and/or defense by worm, mollusk and fish hunting cone snails. Each of the ~700 species of cone snails produces in excess of 1000 different conopeptides, with >99% of the commonly transcribed sequences found in each species still to be pharmacologically characterized. Despite this untapped chemical diversity, conotoxins are already known to target an exceptionally diverse range of membrane proteins, typically with high potency and specificity. Comprehensive integration of transcriptomic and proteomic data has revealed that the vast majority of this conopeptide diversity arises from a more limited set of common genes (~100-400) through a process of variable peptide processing, which generates low levels of conopeptides with alternative cleavage sites, heterogeneous post-translational modifications, and highly variable N- and C-terminal truncations. In addition to this variability around “common” transcripts, a surprisingly large number of distinct conopeptide gene sequences are expressed at low levels, including a series of single amino acid variants, as well as sequences containing deletions and frame and stop codon shifts. Thus, background levels of biological messiness at both the genetic and phenotypic levels in cone snail venom contributes to the extraordinary hypervariability observed for conotoxins. This reservoir of chemical diversity is proposed to facilitate the evolution of conotoxins with new function in response to evolutionary pressure associated with their unique defensive and predatory strategies.