The direct and indirect pathways of the basal ganglia (BG) are classically thought to promote and suppress action, respectively. However, observed coactivation of neurons initiating the two pathways, striatal direct (dMSNs) and indirect (iMSNs) medium spiny neurons, has called this view into question. Here we study these circuits in mice performing an interval categorization task that requires a series of self-initiated and cued actions, and critically, a sustained period of dynamic action suppression. While movement produced similar activation of iMSNs and dMSNs in sensorimotor, dorsolateral striatum (DLS), proactive suppression of action revealed clear signatures of functional opponency between the two pathways as assessed using fiber photometry and photo-identified electrophysiological recordings. Surprisingly, both neural signals and effects of optogenetic inhibition demonstrated that DLS circuits overall were engaged to suppress actions, and not to promote them. Specifically, iMSNs on a given hemisphere were dynamically engaged to suppress contralateral action when that action was tempting. In other words, DLS appeared to support the suppressive complement to an action-promoting policy located elsewhere. To understand how such regionally specific circuit function arose, we constructed a computational reinforcement learning model that reproduced key features of behavior, neural activity, and optogenetic inhibition. The model predicted that parallel striatal circuits not in DLS learned the action-promoting functions that comprise the temptation to act. Consistent with this, optogenetic inhibition in dorsomedial striatum (DMS) indicated that dMSNs there, in contrast to those in DLS, contributed to the promotion of contralateral actions. These data highlight how opponent interaction between multiple circuit- and region-specific BG processes can lead to behavioral control, highlight an underappreciated mode of operation for parallel basal ganglia circuitry, and establish a critical role for the sensorimotor indirect pathway for the proactive suppression of tempting actions.