Transcribed cis-regulatory elements (tCREs), including promoters and enhancers, play a crucial role in gene expression and cell identity. Detailed mapping of tCREs at single-cell resolution is essential to understand the regulatory mechanisms governing cellular functions. Previous tCRE catalogs, limited by bulk analysis, have often overlooked cellular heterogeneity. We have created a tCRE atlas using single-cell 5’-RNA-seq, capturing both gene and tCRE expression from over 340,000 single-cells from 23 human tissues. With more than 175,000 tCREs, this substantially enhances functional cis-regulatory element annotations in the human genome. This atlas unveils patterns of gene regulation, revealing connections between broadly expressed promoters and cell type-specific distal tCREs. We show tCRE are enriched for functional annotations compared to conventional accessibility methods. Assessing trait heritability at the single-cell resolution with a novel tCRE module-based approach, we uncovered the nuanced trait-gene regulatory relationships across a continuum of cell populations, offering insights beyond gene- or accessibility-based methods. Our study bridges the gap between gene regulation and trait heritability, highlighting the potential of single-cell 5’-RNA-seq to elucidate the genetic foundations of complex traits. These insights set the stage for future research to explore the impact of genetic variations in diseases at the individual level, advancing our understanding of the cellular and molecular basis of trait heritability.