Neurons in frontal and parietal cortex encode task variables during decision-making, but causal manipulations of the two regions produce strikingly different results. For example, silencing the posterior parietal cortex (PPC) in rats and monkeys produces minimal effects in perceptual decisions requiring integration of sensory evidence, but silencing frontal cortex profoundly impairs the same decisions. Here, we tested, for the first time, the causal roles of the rat frontal orienting field (FOF) and PPC in economic choice under risk. On each trial, rats chose between a lottery and a small but guaranteed surebet. The magnitude of the lottery was independently varied across trials and was indicated to the rat by the pitch of an auditory cue. As in perceptual decisions, both unilateral and bilateral PPC muscimol inactivations produced minimal effects. FOF inactivations produced substantial changes in behavior even though our task had no working memory component. We quantified control and bilateral inactivation behavior with a multi-agent model consisting of a mixture of a ‘rational’ utility-maximizing agent (U = Vρ) with two ‘habitual’ agents that either choose surebet or lottery. Silencing PPC produced no significant shifts in any parameters relative to controls. Effects of FOF silencing were best explained by a decrease in ρ, the exponent of the utility function. This effect was parsimoniously explained by a dynamical model where the FOF is part of network that performs sensory-to-value transformations.