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Recent theoretical and empirical work has suggested that the X chromosome may play a special role in the evolution of sexually dimorphic traits. We tested this idea by quantifying sex chromosome influence on male relative eyespan, a dramatically sexually selected trait in the stalk‐eyed fly, Cyrtodiopsis dalmanni. After 31 generations of artificial sexual selection on eyespan:body length ratio, we reciprocally crossed high‐ with low‐line flies and found no evidence for maternal effects; the relative eyespan of F1 females from high‐ and low‐line dams did not differ. However, F1 male progeny from high‐line dams had longer relative eyespan than male progeny from low‐line dams, indicating X‐linkage. Comparison of progeny from a backcross involving reciprocal F1 males and control line females confirmed X‐linked inheritance and indicated no effect of the Y chromosome on relative eyespan. We estimated that the X chromosome accounts for 25% (SE = 6%) of the change in selected lines, using the average difference between reciprocal F1 males divided by the difference between parental males, or 34%, using estimates of the number of effective factors obtained from reciprocal crosses between a high and low line. These estimates exceed the relative size of the X in the diploid genome of a male, 11.9% (SE = 0.3%), as measured from mitotic chromosome lengths. However, they match expectations if X‐linked genes in males exhibit dosage compensation by twofold hyperactivation, as has been observed in other flies. Therefore, sex‐linked expression of relative eyespan is likely to be commensurate with the size of the X chromosome in this dramatically dimorphic species.