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Abstract IC 10 X-1 is an eclipsing high-mass X-ray binary containing a stellar-mass black hole (BH) and a Wolf–Rayet (WR) donor star with an orbital period ofP= 34.9 hr. This binary belongs to a group of systems that can be the progenitors of gravitational-wave sources; hence understanding the dynamics of systems such as IC 10 X-1 is of paramount importance. The prominent Heii4686 emission line (previously used in mass estimates of the BH) is out of phase with the X-ray eclipse, suggesting that this line originates somewhere in the ionized wind of the WR star or in the accretion disk. We obtained 52 spectra from the GEMINI/GMOS archive, observed between 2001 and 2019. We analyzed the spectra both individually, and after binning them by orbital phase to improve the signal-to-noise ratio. The radial-velocity curve from the stacked data is similar to historical results, indicating the overall parameters of the binary have remained constant. However, the Heiiline profile shows a correlation with the X-ray hardness-ratio values; also, we report a pronounced skewness of the line profile, and the skewness varies with orbital phase. These results support a paradigm wherein the Heiiline tracks structures in the stellar wind that are produced by interactions with the BH’s ionizing radiation and the accretion flow. We compare the observable signatures of two alternative hypotheses proposed in the literature: wind irradiation plus shadowing, and accretion disk hotspot; and we explore how the line-profile variations fit into each of these models.