Acid soils limit plant production worldwide because their high concentrations of soluble aluminium cations (Al3+) inhibit root growth. Major food crops such as wheat (Triticum aestivum L.) have evolved mechanisms to resist Al3+ toxicity, thus enabling wider distribution. The origins of Al3+ resistance in wheat are perplexing because all progenitors of this hexaploid species are reportedly sensitive to Al3+ stress. The large genotypic variation for Al3+ resistance in wheat is largely controlled by expression of an anion channel, TaALMT1, which releases malate anions from the root apices. A current hypothesis proposes that the malate anions protect this sensitive growth zone by binding to Al3+ in the apoplasm. We investigated the evolution of this trait in wheat, and demonstrated that it has multiple independent origins that enhance Al3+ resistance by increasing TaALMT1 expression. One origin is likely to be Aegilops tauschii while other origins occurred more recently from a series of cis mutations that have generated tandemly repeated elements in the TaALMT1 promoter. We generated transgenic plants to directly compare these promoter alleles and demonstrate that the tandemly repeated elements act to enhance gene expression. This study provides an example from higher eukaryotes in which perfect tandem repeats are linked with transcriptional regulation and phenotypic change in the context of evolutionary adaptation to a major abiotic stress.