Central to all life, gene regulation orchestrates what, where, when, and how genetic information is decoded into biochemical function. This regulation is mediated by non-coding DNA elements, namely promoters and enhancers, that together coordinate the execution of transcriptional programs to shape cellular physiology. Traditionally viewed as distinct in function, promoters initiate gene transcription, while enhancers modulate the levels of gene expression from a distance. However, recent discoveries have blurred this binary classification, revealing that many regulatory elements possess overlapping features and functions. In this dissertation, I explore the fundamental nature of these gene regulatory elements and test the hypothesis that promoters and enhancers are not separate entities but instead represent two manifestations of the same underlying regulatory potential. To investigate this dual functionality, I developed a massively parallel dual reporter assay capable of simultaneously measuring the intrinsic promoter and enhancer activities encoded by the same sequence. Applying this approach to thousands of human genomic elements, I find widespread evidence that both putative promoters and enhancers can exert dual promoter and enhancer functions within the same cellular context, and that promoter activity may be necessary but not sufficient for enhancer function. Using assays configured to simulate promoter- and enhancer-like downstream processing signals, I find that regulatory potential is intrinsic to element sequences, irrespective of features typically associated with these distinct element classes. Perturbing transcription factor binding motifs within elements disrupts both activities, implicating a shared sequence syntax underlying the two regulatory modalities. Combinations of elements with different minimal promoters reveal reciprocal modulation of activity, which, together with a strong correlation observed between promoter and enhancer functions, suggests a bidirectional feedback loop that sustains self-organized environments of high transcriptional output, and validate these phenomena in situ using CRISPR activation at the human β-globin locus. Finally, minimal promoter identity tunes the intrinsic balance between promoter and enhancer functions, while sequence features such as GC content sensitize elements to external regulatory cues, highlighting a context-dependent plasticity in element function. Together, these data indicate that the functional convergence between promoters and enhancers arises from a shared regulatory logic and sequence syntax, advancing a unified model for regulatory element biology. This work provides a new conceptual framework for understanding gene regulation, offering insights into the flexible grammar of the genome’s regulatory code and the functional consequences of regulatory variants in health and disease.