Standing genetic variation and the historical environment in which that variation arises (evolutionary history) are both potentially significant determinants of a populations capacity for evolutionary response to a changing environment. We evaluated the relative importance of these two factors in influencing the evolutionary trajectories in the face of sudden environmental change. We used the open-ended digital evolution software Avida to examine how historic exposure to predation pressures, different levels of genetic variation, and combinations of the two, impact anti-predator strategies and competitive abilities evolved in the face of threats from new, invasive, predator populations. We show that while standing genetic variation plays some role in determining evolutionary responses, evolutionary history has the greater influence on a populations capacity to evolve effective anti-predator traits. This adaptability likely reflects the relative ease of repurposing existing, relevant genes and traits, and the broader potential value of the generation and maintenance of adaptively flexible traits in evolving populations.