Protein evolution is often viewed as smooth hill-climbing, yet reality is defined by rugged landscapes and historical contingency. Building on foundational research by John Oakeshott and Phil Batterham, we dissect organophosphate (OP) resistance in the Australian sheep blowfly. Resistance hinges on a neofunctionalizing mutation (G137D) in the αE7 carboxylesterase, converting it to an OP-hydrolase at the cost of native function. We show this mutation is structurally contingent; it fails in species lacking a specific permissive scaffold. Using directed evolution, we generated a variant with >1000-fold improved turnover. Surprisingly, this evolved enzyme conferred lower resistance in transgenic Drosophila than the natural variant. We resolve this paradox by demonstrating that at physiological toxin concentrations, high affinity (sequestration) is more critical than catalytic turnover. This "OP-sponge" mechanism underscores how biophysical trade-offs between affinity and speed constrain evolutionary adaptation.