Selfish genetic elements occur in all living organisms and often cause reduced fertility and sperm competitive ability in males. In the fruit fly Drosophila pseudoobscura, the presence of a sex-ratio distorting X-chromosome meiotic driver Sex Ratio (SR) has been shown to promote the evolution of increased female remating rates in laboratory populations. This is favored because it promotes sperm competition, which decreases the risk to females of producing highly female-biased broods and to their offspring of inheriting the selfish gene. Here, we show that non-SR males in these SR populations evolved an increased ability to suppress female remating in response to the higher female remating rates, indicating male-female coevolution. This occurred even though SR was rare in the populations. This was further supported by a correlation between females' remating propensity and males' ability to suppress female remating across populations. Thus SR can generate sexual conflict over female remating rate between females and the noncarrier males that make up the majority of the males, promoting evolution of increased ability of males to suppress female remating.