Most components in the nucleus are in a state of dynamic equilibrium maintained by the rapid mobility of nuclear proteins within and between compartments. Mobility is believed to reflect transient binding, but the identity of the binding sites and the function of the transient interactions are a matter of debate. Furthermore, we know little about how these processes may be regulated. Here, we investigate the nature and regulation of transcription factor binding and mobility in the nucleus of yeast cells. Using the Ace1p transcriptional activator, we show that nonspecific DNA binding interactions seem to have a role in retarding Ace1p nuclear mobility. Surprisingly, we find that this binding is a regulated process using a chromatin remodeller to speed up Ace1p interactions at nonspecific DNA sites. Our results suggest that transcription factor mobility represents a diffusion-driven, rapid sampling of nonspecific DNA sites, and that chromatin remodellers accelerate this genomic search process.