Manipulation of cotton canopy architecture offers the potential to maximize yield while minimizing inputs. Here we show that the major leaf shapes of cotton at the L-D1 locus are controlled by a Late Meristem Identity1-D1b (GhLMI1-D1b) gene which encodes a HD-Zip transcription factor. Okra leaf GhLMI1-D1b has a 133-bp tandem duplication in the promoter, correlated with elevated expression, while an 8-bp deletion in the third exon of normal leaf GhLMI1-D1b causes a frame-shifted and truncated coding sequence. Virus-induced gene silencing (VIGS) of GhLMI1-D1b in an okra variety was sufficient to induce normal leaf formation. An intermediate leaf shape allele, sub-okra, lacks both the promoter duplication and the exonic deletion. Our results indicate that sub-okra is the ancestral leaf shape of tetraploid cotton and normal is a derived mutant allele that came to predominate and define the leaf shape of cultivated cotton.