Recent experiments on plant defenses against pathogens or herbivores have shown various patterns of the association between resistance, which reduces the probability of being infected or attacked, and tolerance, which reduces the loss of fitness caused by the infection or attack. Our study describes the simultaneous evolution of these two strategies of defense in a population of hosts submitted to a pathogen. We extended previous approaches by assuming that the two traits are independent (e.g., determined by two unlinked genes), by modeling different shapes of the costs of defenses, and by taking into account the demographic and epidemiological dynamics of the system. We provide novel predictions on the variability and the evolution of defenses. First, resistance and tolerance do not necessarily exclude each other; second, they should respond in different ways to changes in parameters that affect the epidemiology or the relative costs and benefits of defenses; and third, when comparing investments in defenses among different environments, the apparent associations among resistance, tolerance, and fecundity in the absence of parasites can lead to the false conclusion that only one defense trait is costly. The latter result emphasizes the problems of estimating trade-offs and costs among natural populations without knowledge of the underlying mechanisms.