Theoretical models predict that sympatric, ecological speciation may be facilitated more readily when so-called ‘magic traits’ are present, linking traits under divergent selection with assortative mating. Such traits might be encoded by pleiotropic genes, that is, genes that affect multiple, apparently unrelated, phenotypes. However, few convincing examples of sympatric speciation exist, and empirical evidence for the role of magic traits in driving such speciation is rare. One of the strongest cases of sympatric speciation is the Howea palms of Lord Howe Island, Australia, comprising the sister species H. belmoreana and H. forsteriana, which have diverged due to soil substrate preferences and flowering time displacement. By carrying out high-throughput phenotyping experiments using 1,830 Arabidopsis thaliana plants with knockouts of candidate Howea ‘speciation genes’, here we investigate the role that pleiotropy may have played in the speciation process. We identify several genes that show signatures of adaptive divergence between the Howea species and demonstrate pleiotropic roles in soil stress tolerance and flowering time, consistent with the Howea speciation scenario – notably, Howea orthologs of the A. thaliana loci At2-MMP, DCL1, RCD1, SAL1, and SIZ1. Empirical evidence is provided, therefore, for a range of pleiotropic genes with the potential to have driven sympatric speciation by generating magic traits which link divergent selection to non-random mating.