- "I think I'm in love with both of you."
- ―Sookie to Eric & Bill[src]
Sookie Stackhouse remains a major character in Season 4.
Sookie and Claudine arrive in the faery realm, which looks like a whimsical, mythological world, complete with glowing magical light-fruit called Lumiere. Claudine introduces Sookie to other faeries. Sookie recognizes Barry and discovers that her grandfather is there. He claims that he's only been there a few hours, but has actually been missing for the past 20 years.
Sookie refuses the Lumiere fruit and notices that something is off about the perfect place. When she attempts to communicate telepathically with her grandfather, the other faeries all hear her. Queen Mab commands her to eat the Lumiere fruit. When Sookie refuses, Mab tries to force-feed it to her. The Queen blames Sookie for letting Bill taste fairy blood and declares that they are now harvesting humans. Sookie somehow deflects Queen Mab with her light powers revealing the glowing realm into a barren wasteland and the faeries as ugly creatures.
Sookie and her grandfather flee. They are aided by another faery who tells them that there are some who don't agree with the Crown. They escape through a portal and land in the cemetery. Sookie’s Grandfather rapidly ages and turns to dust in front of her; an unexpected effect of the Lumiere fruit.
Sookie returns to her home to find a group of contractors remodelling it. She walks in, confused, and they threaten to call the police. Sookie is surprised that Jason is the responding officer. He is just as surprised to see her and explains that she has been gone for over 12 months; those ten minutes in fairyland just cost her a year of her life. Jason explains that people thought that Bill had killed her. Not knowing that she was still alive, Jason--now a full fledged cop--sold her house. Andy is more abrasive than usual because he’s hooked on V and experiencing withdrawal.
Sookie tells Jason that she was in a place where time moves differently; to prove it to him, she gives him their grandfather's watch. At that moment, the sun starts to set and Bill comes to the house, in joyful disbelief that Sookie is alive. Eric arrives moments later, telling Sookie that he alone knew that she was alive and that he never gave up on her. Bill and Eric bicker and Bill commands Eric to leave, which he does, reluctantly. Bill has become the new Vampire King of Louisiana. To save Sookie from questioning, Bill tells everyone that she was on "vampire business". She agrees to go along with the lie, although she explains to him that she was still hurt by his deception and will not forgive him.
Eric reveals that he is the one who bought Sookie’s house, with the intention of making her “his.” ("She's Not There")
Trying to recover her house, she visits Bill at his home but is stopped by his armed guards. After entering the house, Sookie learns that Bill is now the King of Louisiana and is surprised by this. While trying to adapt herself to the changes of Bon Temps, Sookie reunites with Tara again and gets furious when she discovers that Eric has built himself a cubby in her home. After failing when trying to convince Pam to intercede for her with Eric, Sookie returns home and along the way, Eric stops in his tracks and takes a deep whiff of the night air. He walks up to Sookie's car and looks at her with new and very intense interest. "Why do you smell so good?" ("You Smell Like Dinner")
After discovering that something is wrong with Eric, Sookie takes him home and calls Pam, who explains to her about the witch situation and asks her to care for Eric since she believes that this was set up by Bill to kill him. Sookie reluctantly agrees and then looks for Alcide to help her with Eric's situation but is shocked to learn that a "restored" Debbie was back with him. Sookie arrives home late at night and instead of finding Eric, she finds Claudine at her front porch, who urges her to come back to Faery. Just then Eric swoops up Claudine in a flash and begins to feed on her, killing her in seconds. ("If You Love Me, Why Am I Dyin'?")
Eric, drunk off of Claudine's blood, begins to play with Sookie and disappears in the night. Sookie calls to Alcide for help and that morning they find Eric swimming during daylight in a nearby swamp. Sookie makes him get out of the water as the Fairy blood in his system starts to wear off and the two return home. When Bill approaches Sookie's home looking for Eric, he threatens to come into her home and look for Eric, but she stops him. She tells him that she has never once lied to him, and Bill believes her. He leaves without searching for Eric. ("I'm Alive and on Fire")
After waking in bed to see Eric standing above her with his fangs out after having a nightmare, Sookie comforts him and lets him sleep in the bed with her until daylight. Wanting to solve Eric's problem, Sookie interrogates Holly and later goes to the Moon Goddess Emporium and asks Marnie for a reading. Marnie channels Gran, who tells Sookie to run away from the witch, so Sookie does. After returning home, Sookie comforts Tara after her girlfriend breaks up with her and then Eric appears from his cubby and Tara yells at Sookie by lying and calls out all the atrocious things Eric has done to them. Eric is surprised and tells Sookie he can't be responsible for "snuffing out her light", and begins to leave. He is walking away from the house when Sookie yells out to him. She welcomes him back with open arms and holds him before kissing. ("Me and the Devil")
Eric and Sookie are in the middle of their kiss when Bill barges in and arrested Eric on the grounds of treason and that he has been infected by Marnie. Sookie goes to Bill's home and begs for his release, but Bill is defiant. Later, Sookie visits Jason only to find him handcuffed to his bed. He tells her that he is turning into werepanther form. She stays with Jason through the night, but loses him. She goes into the woods with a rifle and runs into Alcide and Debbie. She asks about werepanthers, and Alcide informs her that werepanthers are only born into creation. Later, Eric surprises Sookie in the woods. He tells her that Bill let him go. The two embrace, and begin to make love. ("I Wish I Was the Moon")
Sookie and Eric made their way to the house without detach from each other and Sookie admits that she would never have allowed the old Eric into her bed. After Bill warns them about an old witch named Antonia Gavilán de Logroño that had risen in Marnie's body and wanted to call all vampires into the sun, Sookie chains Eric with silver to his bed to prevent his death. ("Cold Grey Light of Dawn")
After saving Eric, Sookie offers him her blood to help heal his wounds and Eric begins to feed from her, only to later make her feed from his blood and to start having sex under its influence. Sookie and Eric imagine themselves in a large bed with the snow falling over them in a white forest and when Eric expresses his desire to stay in the state he was in forever, Sookie sadly remarks that there is no such thing as "forever". Sookie persuades Eric to help Bill to fight Antonia, and a battle between witches and vampires is unleashed in the cemetery of Bon Temps, with Sookie, Bill and the other vampires on one side; and Antonia, Tara and other witches on the other. In the midst of the battle, Sookie gets shot in the stomach and falls to the ground seemingly dead, only to be rescued by Alcide. ("Spellbound")
Alcide carries Sookie away from the battlefield. As he runs Bill intercepts him and grabs Sookie. Bill brings her to her house and lays her on the sofa and tries to get her to drink his blood. Bill tells Alcide they have to pray as she barely has a pulse. ("Let's Get Out of Here")
Sookie wakes up; Bill's blood saved her. She instantly asks where Eric is and barely acknowledges Alcide's presence, much less the part he had in saving her life. Alcide is frustrated with Sookie and angrily leaves her home. ("Let's Get Out of Here")
A convalescent Sookie dreams of a world where there is room for both Bill and Eric. Sookie claims to be in love with both of them and the three begin to have sex. ("Let's Get Out of Here")
Debbie surprises Sookie with a visit. She brings her flowers and Sookie reluctantly lets her in. They sit at the kitchen table and Debbie tells Sookie she wants to mend their relationship. She offers her help. Sookie uses her telepathy and believes that Debbie is being honest. She accepts her offer. ("Let's Get Out of Here")
At the Moon Goddess Emporium, Debbie knocks on the door and Antonia answers. Debbie claims to pledge the werewolf's allegiance to the witch's cause. Meanwhile, Sookie is breaking in through a back window. Debbie causes a distraction while Sookie searches for Eric. She finds him in a dazed state, realizing he is under a spell. Tara, wielding a gun, tells Sookie to leave. She telepathically tells Sookie that Antonia is holding them captive, plus where Bill is. They stage a fight so that Tara wouldn't look like a traitor, and Sookie drives away with Debbie. ("Let's Get Out of Here")
Later, Sookie gets to the festival just as they are introducing Bill. Antonia and the other witches are watching in the wings. Bill begins to make his speech when Sookie screams Bill's name. The 3 human security guards are gutted and hanging from the grips of Blackburn, Kirsh and Duprez. The people panic and begin to run and then Sookie screams to Bill to "RUN!" ("Let's Get Out of Here")
As the carnage managed by Marnie/Antonia goes on, Bill and Eric start to fight and Sookie tries to stop them. Forced by the situation, Sookie uses her fairies powers in front of everyone to avoid losing her two loves and breaks Antonia's curse over Eric making Eric regains all his memories. She later confess to him that she still has feelings for Bill but that she was in love with him too. When Bill decides to end the Marnie situation once for all by blowing up the Moon Goddess Emporium, Sookie refuses the idea arguing that there were innocent people caught inside and decides to rescue the hostages on her own. With the help of Lafayette, Jesus and Jason, Sookie learns that Marnie has gone insane and is now the one in charge of the situation. When she tries to help Tara and Holly escape the after the protection spell was broken, Marnie stops them and Sookie is transported into Moon Goddess with everyone else.("Burning Down the House")
Now trapped inside of the Moon Goddess Emporium with everyone else, Sookie tries to reason with Marnie and warns her about Bill's plan. However Marnie refuse to listen as her insanity start to grow and then kills one of the hostages. When Bill, Eric, Pam and Jessica show up to blow up the emporium, Jason tells them about Sookie being abducted and then Bill and Eric reconsider their plan, much to Pam's dismay. They try to reach an agreement with Marnie, who uses Sookie as a shield and orders them to kill each other in exchange for Sookie and the others. Bill and Eric accept her request but Pam refuses to let Eric die for Sookie and shoot Marnie’s protective barrier around the Moon Goddess Emporium with a bazooka, causing Eric to get furious that she endangered Sookie and sends her away.
Marnie convinces everyone that the vampires would not hesitate to kill them and that they need to strengthen the barrier, so they join forces again and begin to recite a spell, including Sookie. However this was only a trick made by Marnie to make the vampires walk to the barrier, which is revealed to be made of the sun’s power. Jason tries to stop them and then telepathically communicates with Sookie and urges her to stop. Overwhelmed by the situation, Sookie summons her powers and breaks the spell again, angering Marnie, who decides to kill her by burning her alive. However, Jesus and Lafayette manage to break the bond between Marnie and Antonia just in time and save Sookie. Bill and Eric confront Marnie and kill her with a shot in the head.("Soul of Fire")
With Marnie dead, the situation seems calm again and Sookie begins to be confused because of her mixed feelings for both vampires. The situation is more stressed when Alcide confesses his love for her after he breaks up with Debbie and reminds her that she would never be happy around Bill or Eric.
However, on Halloween night, Tara informs Sookie and Holly that Marnie now inhabits Lafayette's body and that she has killed Jesus. Worried about the safety of Bill and Eric, Sookie and her friends go to Bill's mansion where they see both vampires about to be burned at the stake. They confront Lafayette/Marnie, who sets a fire around Bill and Eric using the power of the demon who was inside of Jesus. Sookie fairy-light-hands Marnie and knocks her down while the three girls join hands and start to recite a spell that call up the dead of Bon Temps to help.
Sookie is touched when she sees her Grams again and with the help of Adele and Antonia, Marnie is defeated and leaves Lafayette's body, crossing to the light. Sookie pleads with her Grams to stay, but Adele tells Sookie that she can't and advises her about her problem with the two vampires. So to help the two vampires, she holds her arms out, and she allows Eric and Bill to feed off her arms.
Finally, after letting the two vampires feed on her arms, and on the advice of her grandmother, Sookie follows her heart and breaks up with the two after confessing her love for both.
Brokenhearted, Sookie returns to her home only to be confronted by Debbie Pelt with a shotgun. Debbie blames Sookie for all her problems with Alcide and tries to kill her once and for all, but just as she shoots, Tara comes in and pushes Sookie to save her life, getting shot in the head and causing her brain to spread throughout the room. Tara lay on the floor and then Sookie, shocked and in anger by the death of her best friend, knocks out Debbie and the two start to fight on the floor, ending in Sookie having the upper hand. Sookie takes the shotgun and points Debbie on the head, who pleads for her life, but Sookie shoots and kills Debbie instantaneously.
Sookie then returns to where Tara was and takes her in her arms, yelling and screaming for someone to help.("And When I Die")