Cornelius Fudge visits the Muggle Prime Minister to discuss the return of Lord Voldemort and the recent spate of disasters, affecting both Muggles and wizards, that he’s caused. Fudge reveals that he’s been pushed out of office for his inability to contain the Dark wizard and introduces his new successor, the tough and brusque Rufus Scrimgeour.
In another part of England, Narcissa Malfoy clandestinely visits Severus Snape, reluctantly accompanied by her sister Bellatrix. Narcissa begs Snape to aid her son Draco with a mysterious task the Dark Lord has assigned him, and Snape agrees. When Bellatrix questions the wisdom of trusting him, Snape explains how he’s served Voldemort over the years and that he’s been acting as a spy for his entire time at Hogwarts.
Meanwhile, Dumbledore picks Harry up from the Dursleys’, where he’s been mourning his godfather Sirius’s recent death. He takes Harry with him to persuade an old colleague, Horace Slughorn, to come out of retirement and teach at Hogwarts. Slughorn is clearly attracted by Harry’s fame and mystique, and Dumbledore warns him not to be “collected” by the wily professor. Before dropping Harry off at the Burrow, Dumbledore announces that he’ll be giving him private lessons this year and warns him that the Weasleys have received special Ministry security for his protection, and that he must be especially careful about his safety. Harry spends the rest of the summer at the Burrow with Ron and Hermione, but their time together is marred by news of death and disturbance brought by other members of the Order of the Phoenix.
While buying school supplies at Diagon Alley, Harry, Ron, and Hermione encounter Draco Malfoy and clandestinely follow him to the seedy secondhand store Borgin and Burkes, where he speaks with the owner Borgin about repairing a mysterious object and threatens him with unknown consequences if he’s unable to accomplish the task. Harry is convinced that Malfoy has become a Death Eater, but the others don’t believe him. On the Hogwarts Express, Harry eavesdrops on Malfoy bragging about serving Voldemort, but Malfoy catches him, breaks his nose, and traps him in a train compartment, making him late to the school’s first banquet.
To Harry’s surprise and horror, Dumbledore announces that the new Professor Slughorn will be teaching Potions, while Snape will get the job he’s always coveted – Defense Against the Dark Arts. All the sixth-years are overwhelmed by this year’s workload, but Harry is assisted in Potions by a mysterious secondhand textbook he finds in the classroom, which is filled with annotations from a student called the “Half-Blood Prince.” Despite Hermione’s manifest disapproval, the Prince’s notes help Harry become an expert potion-maker. This increases Slughorn’s fascination with him and the professor continually invites him and Hermione to special parties in his office, while conspicuously ignoring Ron. At the same time, Harry is made Captain of the Quidditch team. While the blustering and arrogant Cormac McLaggen tries out for Ron’s position as Keeper, he’s foiled by Hermione, who discreetly Confunds him from the stands.
Harry expects to be learning complicated defensive magic in his lessons with Dumbledore, but instead the headmaster uses the Penseive to show him various memories he’s collected, illuminating Voldemort’s family history and youth. Over many sessions, Harry learns that Voldemort comes from the Gaunt family, who were once wealthy and prestigious but descended into poverty and mental instability. In the Penseive he sees Voldemort’s grandfather, Marvolo, and uncle, Morfin, terrorize his mother, Merope; Dumbledore explains that after the two men are now imprisoned in Azkaban. Merope uses her magic to cast a love charm over a Muggle with whom she’s in love, Tom Riddle Sr. After they are married and she gets pregnant, she lifts the charm, hoping that he’s developed real feelings for her, but he abandons her and she dies of despair shortly after giving birth to their son. Harry witnesses Dumbledore retrieve the young Tom Riddle from the orphanage where he grew up and where the matron reveals his strange abilities and sadistic tendencies. Harry also sees a partially-obscured memory of Professor Slughorn’s in which Riddle asks the professor for information about Horcruxes. Dumbledore explains that Slughorn has tampered with the memory in order to avoid revealing an act of which he’s ashamed, and charges Harry to extract the real memory from him.
Meanwhile, a series of disturbing events are threatening the safety of students at Hogwarts. A member of the Gryffindor Quidditch team, Katie Bell, is placed under the Imperius Curse by an unknown person and charged to deliver a strange package to Hogwarts. When she accidentally touches the cursed necklace inside, she almost dies and spends several months at St. Mungo’s Hospital. Shortly thereafter, Ron accidentally ingests a love potion that Romilda Vane intended to use on Harry. Professor Slughorn mixes an antidote and then offers Ron a glass of mead, but the drink turns out to be poisoned, and only through Harry’s quick action is Ron saved. Harry is sure that Draco and Snape are behind these failed plots, but Ron and Hermione are unconvinced, and when Harry voices his speculations to Dumbledore and McGonagall they reprimand him for making accusations without evidence.
While all of this is occurring, the trio of friends face new romantic challenges. Ron and Hermione seem to be taking a new interest in each other and she wants to invite him to Slughorn’s Christmas party, but Ron is frustrated by the professor’s lack of regard for him and picks a fight with Hermione. Hermione takes Cormac McLaggen, Ron’s Quidditch competitor, to the party instead and Ron starts dating Lavender Brown, whose public displays of affection annoy Harry and hurt Hermione deeply. Meanwhile, Harry and Ron encounter Ginny and Dean Thomas kissing in a corridor. Ron accuses his sister of behaving inappropriately and she explodes, reminding him that he has no business trying to control her love life. Harry realizes that he has feelings for Ginny, but is afraid to act on them after seeing how Ron reacted to Dean.
With so much going on in his life Harry neglects to secure Slughorn’s memory and is reprimanded by Dumbledore for not giving his full attention to such an important task. Ashamed, he drinks a bottle of Felix Felicis, a luck potion he won earlier in a Potions contest. Guided by temporary luck, Harry attends the acromantula Aragog’s funeral at Hagrid’s cabin, encountering Slughorn on the way and bringing him along. Slughorn and Hagrid get extremely drunk and Harry capitalizes on his sentimental mood to persuade him that revealing the memory would be a heroic act. Once he’s obtained the memory, Harry rushes to Dumbledore’s office, where they view Slughorn telling Riddle about Horcruxes, a kind of Dark magic that enables a wizard to split his soul and achieve immortality. Dumbledore hypothesizes that Voldemort has created several Horcruxes and hidden them in various places; it’s imperative to destroy them so that, once defeated, Voldemort will never be able to rise again.
Still suspicious of Draco despite Dumbledore’s reassurances, Harry begins stalking him around the castle. One day he encounters his rival sobbing in a bathroom and confiding in a ghost, Moaning Myrtle, that he fears Voldemort will kill his family if he doesn’t accomplish some task. When Draco catches sight of Harry, they begin dueling and Harry uses an unknown spell from his Potions textbook which turns out to slash Draco’s body, almost killing him. In retaliation, Snape gives Harry detention every Saturday, meaning he has to miss the Gryffindor Quidditch final. Everyone is angry with him, but the team still manages to win the game; in the celebratory aftermath, Harry kisses Ginny in the common room and they begin dating, with Ron’s reluctant approval.
Harry spends several weeks enjoying his new relationship with Ginny before Dumbledore tells him that he’s deciphered the location of one of Voldemort’s Horcruxes and invites him to come on the mission to destroy it. The two Apparate to a remote seaside cave, where Dumbledore uncovers the entrance to a hidden lake. Rowing out to an island in the center, they find a Horcrux – the locket of Slytherin – lying in a basin of liquid. Dumbledore is forced to drink the potion, which weakens him physically and causes him to hallucinate unknown but terrifying delusions. Harry has to spearhead their retreat across the lake, which turns out to be filled with Inferi, or enchanted dead bodies. Supporting Dumbledore, he leaves the cave and Apparates to Hogsmeade, where Madam Rosmerta is awake and points out that the Dark Mark has appeared over Hogwarts – meaning that there are Death Eaters inside.
Borrowing brooms from Rosmerta, Harry and Dumbledore fly to the Astronomy Tower, which is closest to the mark. Dumbledore immobilizes Harry, who is under his Invisibility Cloak, protecting the teenager but leaving himself more vulnerable. Soon Draco emerges onto the ramparts and announces his intention to kill Dumbledore. He reveals that he’s been charged with this task by Voldemort and that he’s behind the cursed necklace and poisoned mead. Despite his bravado, he seems scared and uncertain, and Dumbledore urges him to switch sides, promising to protect him and his family. Several other Death Eaters come into view, among them Snape; the professor raises his wand at Dumbledore and kills him.
Released from Dumbledore’s spell with his death, Harry runs downstairs in pursuit of Snape. When he repeatedly tries to curse him, the professor taunts him and reveals that he is actually the Half-Blood Prince. Then he Disapparates and escapes, along with Draco. Members of the Order of the Phoenix have arrived and dispatched the other Death Eaters, and Harry runs to the hospital wing where they are gathered, grieving Dumbledore’s death and caring for Bill Weasley, who has been mauled by the werewolf Fenrir Greyback. Seeing how devoted Fleur is to her fiancé, Mrs. Weasley reconciles with her future daughter-in-law.
After Dumbledore’s death and the new security breach, Hogwarts’ future is uncertain, but all the students stay for the headmaster’s funeral. The entire Wizarding community descends on campus for the event, which is also attended by magical creatures like merpeople and centaurs, with whom Dumbledore cultivated good relations. Harry feels numb throughout the ceremonies. He realizes that no adult can protect him from Voldemort, and it was a foolish illusion ever to have relied on authority figures. After the funeral he breaks up with Ginny, telling her that he doesn’t want the Death Eaters to use her to get to him. She doesn’t want him to protect her, but ultimately accepts his choice.
Harry tells Ron and Hermione that even if Hogwarts reopens, he’s going to leave school and search for the Horcruxes. He anticipates making this journey alone, but his friends immediately vow to accompany him. Ron tells him that before setting off, they have to return to the Burrow and celebrate Bill and Fleur’s wedding. Harry feels slightly cheered to know that even in this new era of instability, positive things like weddings can still happen. Even though the path ahead is treacherous, he’s bolstered by the thought that he’ll be traveling it with his two best friends.