The dentate gyrus plays critical roles both in cognitive processing and in regulating propagation of pathological, synchronous activity through the limbic system. The cellular and circuit mechanisms underlying these diverse functions overlap extensively. At the cellular level, the intrinsic properties of dentate granule cells combine to make these neurons fundamentally reluctant to activate, one of their hallmark traits. At the circuit level, the dentate gyrus is one of the more heavily inhibited regions of the brain, with powerful feedforward and feedback GABAergic inhibition dominating responses to afferent activation. In pathologic states such as epilepsy, disease-associated alterations within the dentate gyrus combine to compromise this circuit’s regulatory properties, culminating in a collapse of its normal function. Through the use of dynamic circuit imaging and electrophysiological brain slice recordings, pharmacology, immunohistochemistry, and a pilocarpine model of epilepsy, I characterize the emergence of dentate granule cell firing properties during brain development and then examine how the circuit’s normal activation properties become corrupted as epilepsy develops. I find that, in the perinatal brain, dentate granule cells activate in large numbers. As animals mature, these cells become less excitable and activate in extremely sparse populations in a precise, repeatable, frequency-dependent manner. This sparse activation is mediated by local circuit inhibition and not by alterations in afferent innervation of granule cells. Later, in a pilocarpine model of epilepsy, I demonstrate that normally sparse granule cell activation is massively enhanced during both epilepsy development and expression. This augmentation in excitability is mediated primarily by local disinhibition, and the mechanistic cause of this compromised inhibitory function varies over time following epileptogenic injury. My results implicate a reduction in chloride ion extrusion as a mechanism compromising inhibitory function and contributing to granule cell hyperactivation specifically during early epilepsy development. In contrast, we demonstrate that sparse dentate granule cell activation in chronically epileptic mice is rescued by glutamine application, implicating compromised GABA synthesis as a mechanism of disinhibition in chronic epilepsy. We conclude that compromised feedforward inhibition within the local circuit is the predominant mediator of the massive dentate gyrus circuit hyperactivation evident in animals during and following epilepsy development.