Cyclotides are knotted, head-to-tail cyclised peptides comprising of around 30 amino acids. They are currently being exploited as ultrastable scaffolds for the production of peptide-based pharmaceuticals due to their exceptional stability. Cyclotides also merit utility in agriculture as they exhibit insecticidal activity, a role in which they are hypothesised to have evolved for. To date, cyclotides are reported in five angiosperm families. Of particular interest in this study, are the cyclotides found in butterfly pea (Clitoria ternatea), which is currently the only species in the legume plant family that is known to produce cyclotides. Why the butterfly pea cyclotides are produced in such great abundance, and how these are produced and metabolised, are not well understood. To shed light on these questions, the peptide profiles of over a hundred seed-grown butterfly pea accessions were compared; and the promoter region of the most highly-expressed cyclotide (CterM) in the vegetative tissues was characterised. Results showed that the different accessions have variable cyclotide expressions—some of which do not produce CterM. Further scrutiny revealed that these incurred numerous missense mutations, and variability in the regulatory elements, likely contributing to the lack of CterM expression. The promoter region showed numerous binding sites for WRKY, NAC;NAM and EIN3 transcription factors, recapitulating on the hypothesis that cyclotides are indeed metabolised for plant defence. The results also revealed that there are two unique CterM promoters, hinting to the possibility of having two CterM versions—which may either be located in the same loci or different genomic regions.