Towers of Midnight begins with a confrontation between Perrin and Slayer in the Wolf Dream. Perrin’s progress to Caemlyn is blocked by Galad and the White Cloaks, who still want Perrin to face justice for killing two White Cloaks during the Two Rivers’ folks flight from Shadar Logoth. Not wanting to needlessly kill warriors who will be needed at The Last Battle, Perrin attempts to come to a peaceful resolution with the White Cloaks, but battle seems unavoidable. However, when Galad discovers that his stepmother Morgase is alive and posing as a servant in Perrin’s camp, Perrin agrees to be put on trial, with Morgase as the judge.
Morgase finds Perrin guilty in the trial, but Perrin persuades Galad to hold off on passing his judgement until The Last Battle is over. Meanwhile, Perrin discovers that Slayer is using a device that both traps wolves in the wolf dream and prevents gateways, effectively blocking Perrin from using Traveling to move his forces towards Caemlyn. With the help of Hopper and some other wolves, Perrin confronts Slayer in the Wolf Dream and seizes the device, called a dreamspike, and proceeds to move it away from his location, so that the Asha’man can make gateways to move his people. Perrin makes his way to Tar Valon with the dreamspike, with Slayer in pursuit.
Rand visits the White Tower and informs Egwene that he intends to break the seals on the Dark One’s prison. Rand requests that Egwene meet him at the Field of Merrilor in the Borderlands at a future date. Convinced that Rand’s plan is insane, Egwene persuades the rulers of most of the great nations to bring their armed forces at meet her at the Field of Merrilor to stop Rand from breaking the seals.
Meanwhile, Egwene is attempting to find and capture Mesaana in the White Tower. Gawyn requests that Egwene make him her warder, but she refuses, due to the fact that Gawyn keeps messing up her plans by insisting on protecting her. When Gawyn interrupts one of Egwene’s schemes to trap Mesaana, while battling with a Seanchan assassin, Egwene becomes furious and Gawyn leaves Tar Valon to visit his sister in Caemlyn.
Egwene then switches tactics and decides to draw Mesaana out by arranging an important looking meeting with Wise Ones and Sea Folk Windfinders in Tel’aran’rhiod. Egwene’s plan works and Mesanna and the Black Ajah attack. Mesanna attempts to leave Tar Valon, intending to draw Egwene into a trap, but is unable to travel, because Perrin has moved the dreamspike within range of the Tower. With neither party able to leave the Tower, the two factions are forced to square off. Mesaana temporarily captures Egwene with an a’dam, but Egwene uses her superior knowledge and ability in Tel’aran’rhiod to escape the a’dam and break Mesaana’s mind.
While Egwene is battling with Mesaana in the dream world, Gawyn learns from a captured sul’dam in Caemlyn, that the assassin he fought in the Tower was sent by the Seanchan, not by Mesaana and Gawyn rushes back to Tar Valon via a gateway to warn Egwene. Gawyn arrives just in time, as three assassins are closing in on a sleeping Egwene. Gawyn manages to barely fight off the assassins. When Egwene wakes, she discovers Gawyn is badly injured and bonds him as her Warder in order to keep him alive long enough to be healed.
In the Wolf Dream, Slayer kills Hopper, but Perrin is able to destroy the dreamspike by throwing it into a lava pit created by a nightmare and then escapes Slayer be returning to the real world. Perrin discovers that the trap the Forsaken had intended to snare Perrin’s army in, is about to be sprung on the White Cloaks and decides to use his army to save them. Because of his efforts in the battle, Galad decides to pass a light sentence on Perrin. An infuriated Byar attempts to kill Perrin, but Dain Bornhald, who was convinced during Perrin’s trial that he did not kill his father, kills Byar instead. Graendal, who had been responsible for the dreamspike and the failed attempt to destroy Perrin and his army, is punished by Shadar Haran for her failure and her role in Mesaana’s death, due to the dreamspike being taken to Tar Valon.
Back in Caemlyn, Matt finally meets up with Elayne, after another run in with the Gholam. Matt makes a bargain with Elayne to get his dragons put into production. As part of the bargain, Matt agrees to lend the Band of the Red Hand’s services to the defense of Andor, allows Elayne to study his foxhead medallion and attempt to copy it and agrees to split the dragons with Elayne. Elayne succeeds in making some imperfect copies of the medallion, which Matt uses in a trap he set for the Gholam. With the help of some of the Band members and one of the Kinswomen, Matt manages to cause the Gholam to fall into a skimming gateway.
Perrin makes his way back to Caemlyn and Elayne learns that her mother is still alive, but has renounced the throne. Morgase convinces Elayne to allow Perrin to be an official lord in the Two Rivers. Elayne impresses some of her rivals for the Cairhien throne with a display of the dragons’ power and manipulates them into helping her secure the throne of Cairhien.
Though Perrin’s clash with Slayer in the Wolf Dream has helped him to accept the wolf part of his nature, Perrin mourns the loss of his friend Hopper and attempts to bring him back in the Wolf Dream, but fails. Before his death, Hopper instructed Perrin to seek out a wolf named Boundless. Perrin finds Boundless and discovers that he is the man named Noam, that Perrin set free long ago, believing the man had been consumed by the wolf. Perrin learns that Noam actually chose to live as a wolf, instead of a man, because his life as a man had been so difficult and full of pain. This greatly reduces Perrin’s fear that he will someday be consumed by the wolf and cease to be a man.
Aviendha encounters a strange woman on the way to Rhuidean, who causes her to question whether the A’iel should continue with their traditions and return to the three-fold land, now that the purpose behind those traditions is gone. She uses her unique ability with ter’angreal to pass through the glass columns in Rhuidean a second time and the columns reveal to her a possible future in which Aviendha and Rand’s children touch off a series of events that will lead to the destruction of the A’iel and the fall of the White Tower and much of the rest of the world to the Seanchan. Aviendha is horrified by what she sees in the columns and determines to attempt to find a way to prevent the future she has seen from happening.
Matt, Thom and Noal enter the Tower of Ghenjei, hoping to rescue Moiraine. The three take along fire, musical instruments and iron weapons to assist in their confrontation with the Aelfinn and the Eelfinn. When they have difficulty navigating in the tower, Matt uses his luck to choose their path and the three are eventually able to reach the Chamber of Bonds, where he hopes to make a binding bargain that will allow him to escape the tower with Moiraine.
Matt discovers Moiraine a prisoner in the Chamber of Bonds and realizing the meaning of the foretelling he received that he would “Give up half the light of the world to save the world,” agrees to allow the Eelfinn to take one of his eyes, in exchange for safe passage out of the Tower with Moiraine. Unfortunately, Matt forgets about the Aelfinn when he makes his bargain, which only ensures that the Eelfinn will not attack, and the Aelfinn block Matt and his friends from escaping the Tower. Noal, who is really Jain Farstrider, sacrifices himself to hold off the Aelfinn long enough for Matt and Thom to attempt to escape with Moiraine. Unfortunately, Matt is unable to find a way out of the Tower and resigns himself to dying in the Tower, before it occurs to him that the ashandarei he received from the Eelfinn is actually a key that will allow him to escape the Tower. Matt uses the key to open an exit and escapes the Tower with Thom and Moiraine. After their escape, Moiraine reveals that the Eelfinn fed off her ability with the One Power, leaving her capacity greatly diminished, though she was able to mitigate this by making a bargain with them that gained her a powerful angreal that allows her to channel at a much greater capacity than before she was imprisoned, even though unaided, she is no longer strong enough to even be raised as an accepted. Moiraine also reveals her feelings for Thom and the pair agree to get married.
Egwene, Elayne, Perrin and the rulers of most of the powerful nations all converge on the Field of Merrilor to either aid or attempt to stop Rand from breaking the seals on the Dark One’s prison.
Back at Caemlyn, after unexpectedly winning the game of Snakes and Foxes, Olver discovers and decides to open the letter Verin gave to Matt. Talmanes reads the letter and learns that Verin had thought Matt would open it after only a few days and had included a warning that a large force of Shadowspawn were converging on Caemlyn via the Ways. Verin’s letter warns Matt to convince Elayne to destroy the Waygate before they arrive.
Talmanes rushes off, sword drawn, only to discover that Caemlyn is already under attack. Talmanes marshals the Band to defend Caemlyn and prevent the dragons from falling into enemy hands.