The mosquito, Aedes aegypti, spreads viruses that cause dengue, yellow fever, and other devastating diseases. To identify candidate repellents that suppress blood feeding by Aedes aegypti, we conducted an in vitro screen of natural chemicals for activators of two visual opsins, Op1 and Op2, which we found are expressed at very high levels in gustatory organs. We found that Op1 and Op2 are chemical sensors since they are activated by flavonoids, including catechin. We devised an artificial membrane that mimics multiple properties of skin (VectaDerm), which we used on blood feeders, leading to the demonstration that catechin suppresses blood feeding. This behavior was disrupted in op1,op2 double mutants and in trpA1 mutants. High catechin concentrations directly activated TRPA1 and suppressed blood feeding independent of the opsins, while suppression by lower catechin levels depended on the opsins and TRPA1. Roles for opsins and TRPA1 in avoiding catechin are conserved in Drosophila. TRPA1 expressed in the tick vector for Lyme disease, Ixodes scapularis, is also activated by catechin, and I. scapularis is repelled by catechin. Since catechin is safe to humans, we propose that it could be added to repellent formulations to more effectively suppress biting by mosquitoes.