In the yeast Saccharomyces cerevisiae, the decision to mate or invade relies on a shared transcription factor, Ste12. Specificity toward invasion is attributed to Ste12 binding cooperatively with the co-factor Tec1. Here, we show that single mutations in the DNA-binding domain of Ste12 suffice to shift the preference of yeast cells toward either mating or invasion, independent of Tec1. Mutations that result in a shift toward each trait define two regions of this domain, implying an alternative DNA-binding mode for each trait. Binding site selections show that Ste12 variants with shifted trait preference indeed favor alternative DNA-binding sites. We identify temperature-responsive Ste12 variants that promote increased invasion of S. cerevisiae only at high temperature, behavior typical of fungal pathogens. Lastly, we show rare Ste12 mutations confer Hsp90-dependent mating, though wild-type Ste12 is not an Hsp90 client. In summary, flexibility in Ste12 DNA-binding mediates an environmentally-sensitive control of two complex traits.