Genji is the son of the Emperor and Kiri-Tsubo, the Emperor's beloved mistress. Kiri-Tsubo lacks powerful connections and is often the subject of jealous attacks by others at court, some led by the another of the Emperor's mistresses, Lady Koki-den. Genji’s mother and grandmother die when he is a child and the bereft Emperor brings his son into the palace to oversee his education. His glittering future is foretold both by his personal gifts and by a Korean ambassador, who reads his future and promises that, as long as he does not seek political power, his life is likely to be one of distinction. When Genji reaches the age of maturity, his father associates his son with the clan of Gen and marries him to the Lady Aoi, a woman from a powerful family. The Emperor selects his and Lady Koki-den's first son as his Heir Apparent. 

Romantic adventure occupies much of Genji’s time as a young man, although he is also a gifted poet, dancer, musician, and painter. He establishes an ongoing relationship with the Lady of Rojukō. but neither this nor his marriage prevents him from pursuing other women who strike his fancy. The list of women he pursues is long—the Princess Wistaria, Cicada, Yūgao, Violet, Princess Hitachi, the older woman at court, Naishi-no-Kami, and the Lady of Akashi—and his success with them is varied. Cicada reluctantly rejects Genji and the older woman and Princess Hitachi prove not to his liking in the end. Throughout all of his adventures, however, his strongest attachments are to the two women who resemble his mother, Princess Wistaria and Violet. Both the Lady of Rojukō and Princess Wistaria eventually retreat from society and become nuns, in part to help them resist Genji. 

Genji’s life is not without its complications. Not only is Lady Koki-den jealous of Genji’s possible place in court, his wife, Lady Aoi, and his mistress, the Lady of Rojukō, are also unhappy about his intrigues. Rojukō is so upset that her spirit attacks Yūgao after she and Genji make love, leaving Yūgao dead. Rojukō’s spite even extends to Lady Aoi. After a disagreement over whose carriage should have priority, her spirit also attacks Genji’s wife. Aoi gives birth to a son but dies a few days later. Genji’s encounter with Naishi-no-Kami, one of Lady Koki-den’s sisters, intensifies her ire and she maneuvers to have Genji sent into exile. Because his father stepped down from the throne before he died, there is no real check on her power. So, although he is prominent, performing at festivals and popular with many at court, she prevails and he leaves for Suma and exile. 

Genji is miserable in exile, missing his friends and lovers. Violet and his friend Tō-no-Chūjō manage to write him, but most people obey the wishes of Lady Koki-den and the new Emperor. Genji fills his empty days with painting, thinking, and talking to fishermen. A dream of his father encourages him to brave the stormy seas. A relative of his mother’s, now a priest at Akashi, tries to persuade Genji to join with his daughter at their home. While there, Genji begins a relationship with the woman, who later gives birth to his daughter. Back at court, the Emperor has also had a dream of his father, who urges him to summon Genji back to the palace. He manages to evade his mother and sends the order. 

Genji’s return paves the way for the resolution of various plot lines. He meets many of the women he had previously seduced (or tried to seduce) and learns about the events that took place while he was away. Cicada’s husband has died, and she is on her way to become a nun. Princess Hitachi had not understood that Genji had lost interest in her and spent years waiting for his return. More mature after his trials, Genji decides to provide her with financial support. Violet is happy that he is home but expresses jealousy about his relationship with the Lady of Akashi, particularly the fact that the woman has given Genji an infant daughter. Finally, an ill Lady of Rojukū asks Genji to take charge of her beautiful daughter. Still attached to her, despite everything, Genji agrees. 

The abdication of Genji’s half-brother places his own (unacknowledged) son on the throne. Genji decides that the young Emperor should be married to the Lady of Rojukū’s daughter. But his friend, Tō-no-Chūjō, hopes to marry the new young Emperor to one of his own children. To decide the issue, there is a competition of paintings, some completed by members of court and others held in their collections. As usual, Genji wins the competition, securing an excellent marriage for his young ward, as he contemplates a possible retreat from the busy life at court. There are 37 more chapters in the full version of The Tale of Genji, but most abridged versions, including the Suematsu translation used here, end with the painting competition.