Summer Knight is the story of Harry Dresden, Chicago native and wizarding detective. Harry is dragged into the affairs of the Summer Court of the faeries when murders and disappearances upset the balance between Summer and Winter. In attempting to track down a kidnapped ward of Summer, Harry discovers a plot by the princess or "Lady" or the Summer Court to usurp her mother's power and annihilate Winter, destroying the balance between the two courts.
Mab, the Winter Queen of the Sidhe, has purchased Dresden’s debt from his fairy godmother, Leanansidhe. She tells Dresden he can pay off his debt by doing three favors. The first favor is for him to find the murderer of the Summer Knight Ronald Reuel and recover his stolen mantle. Dresden refuses her request, but is forced by the White Council to acceptthe role of her Emissary as his Trial, else be stripped of his title of wizard and handed over to the Red Court vampires as a peace offering.
Dresden is visited by Elaine, his former lover, now the Emissary of the Summer Court, indebted to Aurora, the Summer Lady. Dresden goes to Reuel’s funeral, looking for a group of teenage half-human/half-Fae changelings who were Reuel's friends, but they flee and attack, believing him to be in service to Winter. An interview with the sadistic Winter Lady, Maeve, convinces him that she did not kill the Summer Knight.
The changelings ask Dresden to find their friend Lily, and he agrees. He discovers a gravely wounded Elaine and takes her to the Summer Lady. Aurora heals Elaine, but is not forthcoming with any details on Reuel’s murder or Lily’s disappearance. She explains that the death of the Summer Knight and the theft of his mantle of power shifted the power balance in favor of Winter, driving the Summer Court to attack Winter at Midsummer before their power fades.
Dresden summons Leanansidhe, who transports him to an ethereal Chicago-over-Chicago, where a great Stone Table, the sacrificial stone that maintains the balance between the Winter and Summer Sidhe, now rests. The power of blood spilled upon that table will change the balance of power between the Courts. Dresden persuades Elaine to help him reach the Mothers, the elder Queens of Summer and Winter. They goad him into answering his own questions, realizing that Aurora killed the Summer Knight and transferred his mantle to Lily, who she then turned to stone. They give him a Cloth of Unraveling to release Lily.
Aurora ambushes Dresden and takes him prisoner, aided by Elaine and by the Winter Knight, who she has suborned. Aurora intends to ritually sacrifice Lily on the Stone Table, transferring the power of the mantle to the Winter Sidhe and breaking the unending cycle of struggle between the Faerie Courts. Elaine covertly betrays Aurora, leaving Dresden an escape route from Aurora's sorcerous deathtrap. During the battle between the Courts, Dresden confronts Aurora, who dies at the hands of pixies armed by him with cold iron.
Mab offers Dresden the mantle of the Winter Knight, which he declines. Queen Mab grants safe passage to the White Council of the wizards, enabling Dresden to pass his Trial. Lily becomes the new Summer Lady and her changeling friend Fix her new Summer Knight.