Understanding the causes of gene expression variation is of major importance for many areas of biology. While cis-regulatory changes have long been suggested to be particularly important for adaptation, our understanding of what determines cis-regulatory variation remains limited in most species. Here, we have investigated the prevalence, selective importance, and genomic correlates of cis-regulatory variation in the outcrossing crucifer species Capsella grandiflora. We identify genes with cis-regulatory variation through analyses of allele-specific expression (ASE) in deep transcriptome sequencing data from flower buds and leaves, and use population genomic analyses of high-coverage whole genome resequencing data from both a range-wide sample and a natural population to quantify the impact of positive and purifying selection on these genes. Our results show that in C. grandiflora, cis-regulatory variation is pervasive, affecting an average of 35% of genes within individual plants. Genes harboring cis-regulatory variation are (1) under weaker purifying selection, (2) significantly more likely to harbor nearby transposable element (TE) insertions, and (3) undergo lower rates of adaptive substitutions in comparison to other genes. Using a linear model, we identified ASE as the strongest factor contributing to purifying selection when considered alongside several other commonly used contributing factors. In turn, the main genomic correlates of cis-regulatory variation are presence of nearby TE insertions and gene expression level; notably, the signal of relaxed positive and purifying selection on genes with ASE remains after controlling for expression level. Our results suggest that variation in the intensity of selection across the genome is a major determinant of the presence of intraspecific cis-regulatory variation in this outcrossing plant species.