The CarD-CarG complex controls various cellular processes in the bacterium Myxococcus xanthus including fruiting-body development and light-induced carotenogenesis. The CarD N-terminal domain, which defines the large CarD_CdnL_TRCF protein family, binds to CarG, a zinc-associated protein that does not bind DNA. The CarD C-terminal domain resembles eukaryotic high mobility group A (HMGA) proteins, and its DNA-binding AT-hooks specifically recognize the minor-groove of appropriately spaced AT-rich tracts. Here, we investigate the determinants of the only known CarD binding site, the one crucial in CarD-CarG regulation of P(QRS), a light-inducible promoter dependent on the extracytoplasmic function (ECF) factor CarQ. In vitro, mutating either of the 3-bp AT tracts of this CarD recognition site (TTTccagagcTTT) impaired DNA binding, shifting the AT tracts relative to P(QRS) had no effect or marginally lowered DNA binding, while replacing the native site by the HMGA1a binding one at the human interferon-β promoter (with longer AT tracts) markedly enhanced DNA binding. In vivo, however, all these changes deterred P(QRS) activation in wild-type M. xanthus, as well as in a strain with the CarD-CarG pair replaced by CarD(Ad)-CarG(Ad). The latter is functionally equivalent to CarD-CarG despite the lower DNA-binding affinity in vitro of CarD(Ad), whose C-terminal domain resembles histone H1 rather than HMGA. We show that CarD physically associates with RNAP specifically via interactions with the RNAP β subunit. Our findings suggest that CarD regulates a light-inducible, ECF-dependent promoter by coupling RNAP recruitment and binding to a specific DNA site optimized for affinity and position.