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 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. These results are robust to correction for nonequilibrium demography and expression level variation among genes. In a logistic regression model, we identified presence of nearby TE insertions as a major factor increasing the odds of ASE, whereas gene body methylation was a major factor associated with reduced odds of ASE. Our findings suggest that gene body methylated genes are not only strongly conserved at the sequence level but also with respect to cis-regulatory variation. These results suggest that variation in the intensity of purifying selection across the genome, in part determined by gene body methylation, is a major determinant of the presence of intraspecific cis-regulatory variation in this outcrossing plant species.