Classical models of bacterial transcription show regulators binding close to promoter elements to exert their effect. However, the scope for long-range regulation exists, especially by nucleoid structuring proteins, like H-NS. Here, long-range regulation by VirB, a transcriptional regulator that alleviates H-NS-mediated silencing of key virulence genes in Shigella species, is explored in vivo to test the limits of long-range regulation and provide further mechanistic insight. VirB-dependent regulation of the well-characterized icsP promoter persists if its cognate site is repositioned 1 kb, 3.3 kb, and even 4.7 kb further upstream than its native position in a plasmid reporter. VirB-dependent regulation diminishes with binding site distance. While increasing cellular VirB pools elevated promoter activity in all constructs with wild-type VirB binding sites, it did not generate a disproportionate increase in promoter activity from remote sites relative to the native site. Since VirB occludes a constitutively active promoter (PT5) when docked adjacent to its -35 element, we next moved the VirB binding site far outside the promoter region. We discovered that VirB still interfered with promoter activity. These findings and those generated from molecular roadblocks engineered around a distally located VirB-binding site are reconciled with the various models of transcriptional regulation by VirB.