Human cultivation during plant domestication imposed strong selection on fitness relevant traits. The relationship between apparent trait changes and fitness is not always obvious. For instance, seed color changed in numerous crops early during their domestication. In the pseudocereal grain amaranth seed color changed from dark to white three times during its repeated domestication. However, the genetic basis and functional relevance of the seed color change is still unknown. To study the ecological function of seed pigments in grain amaranth, we assessed germination properties in hundreds of lines using a semi-automated phenotyping system and found that white seeds germinate significantly faster than dark seeds. The metabolomic analysis of seeds showed reduced accumulation of flavonoids, including the dark proanthocyanidins, in white seeds. To study the genetic control of the change, we employed genome-wide association mapping and RNA sequencing in diverse accessions. Differential gene expression analysis revealed the downregulation of almost all flavonoid pathway genes in white seeds. The genomic analyses identified the insertion of a transposable element (TE) into a regulator of the flavonoid pigment pathway as one causal mutation for the seed color change. Using full-length transcript sequencing, we show how the TE induces alternative splicing in the regulator which results in loss of function for pigment pathway regulation. We demonstrate how a seemingly fitness-unrelated trait like seed color can confer environmental adaptation and how the insertion of a transposable element altered the expression of a whole metabolic pathway to enable the trait change.