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Balanced mating type polymorphisms offer a distinct window into the forces shaping sexual reproduction strategies. Multiple hermaphroditic genera in Juglandaceae, including walnuts (Juglans) and hickories (Carya), show a 1:1 genetic dimorphism for male versus female flowering order (heterodichogamy). We map two distinct Mendelian inheritance mechanisms to ancient (>37 million years old) genus-wide structural DNA polymorphisms. The dominant haplotype for female-first flowering inJuglanscontains tandem repeats of the 3′ untranslated region of a gene putatively involved in trehalose-6-phosphate metabolism and is associated with increasedcisgene expression in developing male flowers, possibly mediated by small RNAs. TheCaryalocus contains ~20 syntenic genes and shows molecular signatures of sex chromosome–like evolution. Inheritance mechanisms for heterodichogamy are deeply conserved, yet may occasionally turn over, as in sex determination.