Sequencing of whole tumor genomes holds the promise of revealing functional somatic regulatory mutations, such as those described in the TERT promoter. Recurrent promoter mutations have been identified in many additional genes and appear to be particularly common in melanoma, but convincing functional data such influence on gene expression has been elusive. Here, we show that frequently recurring promoter mutations in melanoma occur almost exclusively at cytosines flanked by an extended non-degenerate sequence signature, TTCCG, with TERT as a notable exception. In active, but not inactive, promoters, mutation frequencies for cytosines at the 5' end of this ETS-like motif were considerably higher than expected based on a UV trinucleotide mutation signature. Additional analyses solidify this pattern as an extended context-specific mutational signature that mediates an exceptional position-specific elevation in local mutation rate, arguing against positive selection. This finding has implications for the interpretation of somatic mutations in regulatory regions, and underscores the importance of genomic context and extended sequence patterns to accurately describe mutational signatures in cancer.