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Eric is intrigued when Bill Compton brings Sookie to Fangtasia in her search for clues about murders happening in her hometown of Bon Temps, and his interest is further piqued when Sookie reads the mind of an undercover cop in the bar and is able to alert Bill to an imminent police raid. The two signal Eric and bartender Long Shadow on their way out, and Sookie must admit that she is a telepath when Eric questions how she knew. When he discovers that someone is embezzling from the bar, he orders Bill to bring her back to Fangtasia to read his employees’ minds. When she worries that she could be sentencing a human to death by identifying him, Eric agrees to turn the thief over to the police if she will make herself available for further use. Although she cannot read vampire minds, Sookie does get the image of the embezzler from one of the waitresses and names Long Shadow. Eric is forced to stake his bartender when Long Shadow attacks Sookie. Even though the circumstances made it impossible to turn Long Shadow over to the police as promised, Eric holds Sookie to her end of the bargain.

A maenad passing through the area uses Sookie’s back as a billboard to tell Eric that she expects tribute. Eric arranges for a supernatural doctor to attend to Sookie’s wounds and provide a transfusion, joining Pam, Bill, and new bartender Chow in draining Sookie of most of her poisoned blood. After her recovery, he sends her to Dallas to help locate the missing nest mate of vampire sheriff Stan Davis. Although the deal calls for only Sookie and Bill, Eric decides to go in undercover as a visiting California vampire named Leif. When the Fellowship of the Sun attacks Stan’s house as the vampires are celebrating Farrell’s safe return, Eric takes a bullet while covering Sookie. He uses the situation to his advantage by telling Sookie she must suck out the bullet, even though he knows it will pop out on its own. By getting his blood in her, even a drop, he will have insight into her feelings.

Eric accepts Sookie’s invitation to an orgy but is taken aback when she requests that he pretend to be gay. Their attendance is, of course, a ploy to gain information on the murder of Lafayette Reynold, Sookie’s friend and co-worker at Merlotte’s. Eric shows up at Sookie’s house on time, resplendent in pink and aqua Lycra, and promises to keep her safe. Sookie does discover the killers through their thoughts and Eric gets her out of the immediate situation, but unfortunately for everyone involved, the maenad, Callisto, attends the orgy as well, attracted by the alcohol and debauchery. She sends her madness into the participants, sparing only Sookie, Tara, Eggs, Eric, and a newly arrived Bill, and the vampires clean up the mess afterward.

Eric relies on Sookie’s affection for Bill when Bill goes missing along with a valuable project he was working on for their queen, and he sends werewolf Alcide Herveaux to escort her to Jackson in search of her missing lover. Once again, he shows up on the scene loosely disguised as Leif, coming to Sookie’s aid when she is staked at Club Dead. They are taken to the King of Mississippi’s mansion so she can be healed, and after she confirms that Bill is there, Eric finds her transportation so that she can rescue Bill during the day and escape. In the meantime, Eric spends his time with an adorable vampire named Bernard who has taken a shine to the big Viking. Eric plays along to help facilitate their plan. While Eric drives Sookie back to Bon Temps, the two are attacked first at a gas station by thugs (hired by a biker gang involved with Bill’s captivity) and then by the gang members themselves at Sookie’s home. As payment for Sookie’s services, Eric has her entire driveway repaved.

A witch coven composed mainly of shifters who drink vampire blood comes to Shreveport to try to take over Eric’s business network. He refuses the coven leader’s offer of a better deal if he pleases her sexually and is cursed with amnesia when Chow attacks the witch who delivers the offer. Frightened, confused, and alone, he finds himself running down the road toward Sookie’s house early New Year’s morning and is taken in by a sympathetic Sookie. Jason makes a deal with Pam and Chow for Eric to remain at Sookie’s house as a paying guest while the witches are dealt with, and Eric and Sookie begin a brief, passionate affair. The witches are defeated in a joint effort by the local vampires and local Weres, and Eric and Sookie return to her house because his memory hasn’t yet returned. Upon entering the back door, they are surprised to find Debbie Pelt waiting for them with a gun. Eric steps in front of Sookie to take the bullet, giving Sookie time to grab a shotgun and blow most of Debbie’s head off. Eric disposes of the body and Debbie’s car while Sookie cleans up the mess. He returns in time to kiss her good night and climb into the hidey-hole in her guest room closet. By the time he awakens the next night, his memory is restored, but he has no recollection of what happened while he had amnesia, although he suspects it was more than a simple stay-over at Sookie’s.

When Sam is shot and it’s discovered that shifters are being targeted, he asks Sookie to ask Eric if he can borrow a bartender. Eric readily agrees, always happy to be owed a favor, and sends Charles Twining, a newly hired bartender from Mississippi. Eric is unhappy to learn that Mickey, vampire child of Salome, is in the area and tells Sookie to stay away from him. Tara becomes involved with Mickey, passed to him by another vampire she was dating, and Sookie asks for Eric’s aid again, this time for her friend. Eric uses the favor to call in one from Sookie: He wants to know everything that happened while he had amnesia, and she tells him. In return, he calls Salome to call off her child, who is violating the new rules the vampires are trying to live by. Eric becomes suspicious of Charles Twining and decides to further check his references. To his horror, he discovers that Charles is pledged to Hot Rain, the sire of Long Shadow, and is there to take vengeance on Eric by harming Sookie. By the time he reaches Merlotte’s, the human patrons have taken care of the problem.

Eric is unhappy when he has Pam call Sookie to a meeting and Sookie will not attend as she has a date with weretiger Quinn. Eric goes to her house instead and becomes enraged that not only is Sookie going on a date with the weretiger, but Quinn has delivered the news that vampire Queen Sophie-Anne Leclerq is claiming Sookie’s services for the upcoming vampire summit, usurping Eric. Eric travels separately to New Orleans as Sookie is heading down with Mr. Cataliades to take care of her late cousin Hadley’s apartment and legal affairs, with Bill as a passenger. Eric finds her in the hospital after she is attacked by Jake Purifoy and, when Bill enters as well, forces him to tell Sookie that he was sent by Sophie-Anne to gain her confidence. Because Sookie and he have had each other’s blood, Eric is called upon to track her after she and Quinn are kidnapped. When the melee breaks out at Sophie-Anne’s spring party, Eric slays the Arkansas vampire who decapitated Wybert.

As planned, Eric, Bill, and Sookie all travel to the summit as part of the queen’s entourage. The King of Mississippi and the King of Indiana conclude their marriage contracts and decide to marry at the summit, but the priest doesn’t show up for the wedding. Ordained online by the Church of the Loving Spirit, Eric steps in as priest and performs the ceremony, keeping the ceremonial knife and cloak afterward. When Andre decides to force Sookie into a blood bond to tie her closer to the Louisiana vamps, Eric steps in again and offers himself in Andre’s stead, using the ceremonial knife to cut himself for Sookie. Eric and Pam are saved by Sookie during the bombing of the hotel and return to Shreveport to recover.