Genly Ai, a male Terran native, is sent to represent the Ekumen, the intergalactic coalition of humanoid worlds, on the frozen planet Gethen, also called Winter. Like all envoys of the Ekumen, he can "mindspeak" – a form of quasi-telepathic speech. He finds that apparently the people of Winter cannot mindspeak. After landing in Karhide, a Gethen kingdom, Genly makes little progress, though he seems to have convinced the Karhiddish Prime Minister, Estraven, of the value of joining the Ekumen. The night before Genly's first audience with the king, Ai begins to doubt Estraven's loyalty because of his strange, effeminate ambiguity. The next day, as he prepares to meet the King, Ai learns that Estraven has been accused of treason, and fled to a neighboring country, Orgoreyn. After meeting with the King, who rejects his invitation to join the Ekumen, he explores Karhide. He pays a group of Foretellers for a mystical Foretelling. He asks if Winter will be a member of the Ekumen in five years, and is told that it will be. Later, a leader of the Foretellers explains to Genly why the Foretellers have perfected their art: to prove the uselessness of knowing the right answer to the wrong question. Ai decides to pursue his mission in Orgoreyn.
Where the people of Karhide's actions were dictated by shifgrethor, an intricate set of unspoken social rules and formal courtesy, Orgota are technically organized and practically logical. They provide Ai with comfortable habitations and ask direct questions. He presents his invitation to the Orgota leaders, relieved that he has nearly reached success. Yet, Ai senses an unspoken aura of fear, and Estraven warns him not to trust the Orgota leaders. He ignores both his feeling and the warning, and is once again blindsided. Overnight, Ai is sent to a far-northern work camp to meet his death by cold, labor, and sterilizing drugs.
To Ai's surprise, Estraven—the person Ai least trusts—goes to great lengths to save him. After breaking out of the work camp, the pair begin the unprecedented 80-day trek across the Gobrin Glacier back to Karhide, where Estraven believes they will finally be able to maneuver acceptance of the Ekumen treaty. Only by working together, learning to trust and accept one another's differences, are the pair able to succeed. At one point, Estraven enters kemmer and becomes "female". Ai, who thinks of Estraven as more male than female, essentially ignores the implications of the kemmer. When they reach Karhide, Estraven is killed, and Genly realizes he has lost a beloved friend. Above all, Estraven was loyal to Ai's mission: the greater good of universal humanity, above the personal or patriotic. Through Estraven and Ai's collaboration, and the powerful political fallout of Estraven's death, the mission of the Ekumen is accomplished. Karhide will join the Ekumen, followed by Orgoreyn.