The biology of the extant American horseshoe crab, Limulus polyphemus, is well documented—including its dietary habits, particularly the ability to crush shell with its gnathobasic walking appendages—but virtually nothing is known about the feeding biomechanics of this iconic arthropod. This species is also considered the archetypal functional analogue for a range of extinct groups that have gnathobasic appendages, including eurypterids, trilobites, and some of the earliest arthropods, especially Sidneyia inexpectans from the middle Cambrian (508 million-year-old) Burgess Shale of Canada. Exceptionally-preserved specimens of S. inexpectans show intriguing evidence suggestive of durophagous (shell-crushing) tendencies—including thick gnathobasic spine cuticle and shelly gut contents—but this feeding mode has never been substantiated using advanced computational techniques, such as Finite Element Analysis (FEA). Here we present a unique application of 3D FEA by modelling the feeding mechanics of L. polyphemus and S. inexpectans, representing the first such analysis of a modern horseshoe crab, or indeed any fossil arthropod. Results show that mechanical performance of the feeding appendages in both arthropods is remarkably similar, confirming that S. inexpectans was a durophagous predator. This biomechanical solution to processing shelled prey therefore has a history extending over 500 million years, almost dating back to the first appearance of shell-bearing animals themselves. The arrival of durophagous predators such as S. inexpectans during the early phase of animal evolution undoubtedly fuelled the Cambrian ‘arms race’ that encompasses the rapid increase in diversity and abundance of biomineralised prey species.