Venoms are complex biochemical arsenals, often containing hundreds to thousands of unique proteins and peptides. Despite their utility for prey capture, venoms are energetically expensive commodities, and consequently it is hypothesized that venom complexity is inversely related to the capacity of a venomous animal to physically subdue prey¹. Centipedes, one of the oldest yet least studied venomous lineages, appear to defy this rule². We examined a taxonomically diverse range of centipedes using a multidisciplinary approachthat included proteomics, transcriptomics, MALDI imaging, histology, immunohistochemistry, MRI, mCT, and electron microscopy to provide the first comprehensive insight into the composition and evolution of these ancient and unique venoms. Our results reveal a rich set of both novel and convergently recruited toxin types, but also substantial variation in toxin diversity between higher-order taxa. Surprisingly, despite lacking the formidable physical weaponry of scolopendrid centipedes, scutigeromorph venoms appear relatively non-complex. We show that the observed disparity in venom complexity between scolopendrid and scutigeromorph centipedes likely stem from morphological limitations of the venom gland, and that scolopendrids may be unique among centipedes in having evolved venom glands that can accommodate the peptide diversity characteristic of many arthropod venoms^3,4. Moreover, the same morphological adaptations that allow great venom complexity in scolopendrid centipedes also appears to enable exquisite control over the composition of secreted venom. Our results provide further support for the concept that toxins are not universally expressed throughout the glands of venomous animals, and that this heterogeneity of toxin production can enable modulation of the composition of secreted venom. Our finding of morphological constraint on toxin diversity has substantial implications for centipede venoms as a biodiscovery resource, and our results are a clear example of an interdisciplinary approach to understanding the evolution of venom systems may guide such efforts.