Across a species range, islands of stressful habitats impose similar selection pressures on isolated populations. It is as yet unclear, when populations respond to these selective pressures, the extent to which this results in convergent genetic evolution and whether convergence is due to independent mutations or shared ancestral variation. We address these questions investigating a classic example of adaptation by natural selection – the colonization of plant species to heavy metal contaminated soils. We use field-based reciprocal transplant experiments to demonstrate that mine alleles at a major copper tolerance QTL, Tol1, are strongly selected in the mine environment, but are neutral, or nearly so, in the off-mine environment. To identify scaffolds in genetic linkage with this locus, we assemble the genome of a mine adapted M. guttatus genotype and sequence near isogenic lines (NILs) homozygous for tolerant or non-tolerant alleles at Tol1. We identify genes with differential expression between NILs and differences in allele frequency between independent pairs of mine and off-mine populations to identify Tol1 candidate genes. We identify a single gene, a multicopper oxidase, with large differences in expression between NILs and allele frequency between populations. Furthermore, we find patterns of genetic variation at Tol1, and four additional candidate adaptation loci, are consistent with selection acting upon beneficial haplotypes that predates the existence of the copper mine habitat. We estimate the age of selected Tol1 haplotype to be at least 1700 years old and was at a frequency of 0.4-0.6% in the ancestral population when mining was initiated 150 years ago. These results suggest that adaptation to the mine habitat routinely occurs via selection on ancestral variation, rather than independent de-novo mutations or migration between populations.