Chapter 1: Mike Donovan
The game begins with a narration by Dexter who introduces himself and says that he is going to kill that night. Mike Donovan, upstanding teacher and choir director who seems to have been burying his dirty secrets, Dexter followed Donovan to the outskirts of Miami. After Donovan left, Dexter investigates the area and confirmed his suspicions that Donovan has been killing off his own choir boys and burying their bodies there. Dexter prepares his Kill Room at a nearby building, all it needs is Donovan. Dexter sneaks to the choir stage and snatches Donovan's car keys, Donovan entered his Volvo after a choir performance, where Dexter was waiting in the backseat; after Donovan started the engine, he choked him with a garrote wire and ordered him to drive to the abandoned building from earlier. Dexter wakes up the sedated Donovan and takes a blood slide through a scalpel cut, Dexter makes Donovan confess for his crimes and kills him. Dexter dumps Donovan's remains into the sea and adds his blood slide to his collection.
Chapter 2: Dear Dexter
The game's main plot, this chapter occurs between all the chapters. After dumping Donovan's body out to sea, Dexter returns to his apartment and receives a message from Debra who asked him to get to the Lucky Ocean Motel. Dexter arrives at the scene, having conversations with Debra, LaGuerta, Batista, and Masuka, he then examines a decapitated body with no single drop of blood on it and heads off to the station. After a brief confrontation with Doakes at the station, Dexter brought some donuts to Camilla so that he could get his hands on the latest case files. Dexter then visits Rita and wanted to show her a good time by visiting a crab restaurant she wanted to see, but it was interrupted when he spots a crime scene nearby with the victim being killed in a similar manner as the victim found at the Motel, Dexter then took Rita home. Dexter talks to Debra about her idea that the killer might be using the method of cell crystallization to explain the absence of blood in the victims, which leads to the idea that the killer might be using a refrigerated truck as Debra tries to convince this idea to LaGuerta. Debra later told Dexter of her failure in convincing LaGuerta with the refrigerated truck theory during the briefing, Dexter cheers her up by giving her some confidence and advised her to search for the truck.
Chapter 3: Coke Head
Doakes theorized that the "Coke Head" case was certainly a fight over drugs, but Dexter analyzes the blood spatter found at the crime scene and found that the cuts on the girl were quick and passionate, but the guy was an afterthought. He then presented his findings to LaGuerta, supporting the fact that it was a crime of passion and had nothing to do with drugs. LaGuerta decided that Dexter's theory was more relevant compared to Doakes' and decides to follow Dexter's theory in the investigation. Doakes confronts Dexter and threatens to ruin him if his theory was wrong, however, Dexter simply replies that he isn't wrong because the blood isn't wrong.
Chapter 4: Jamie Jaworski
Dexter suspects Jamie Jaworski to be involved in the murder of Jane Saunders and several other women and decides to spy on him at the Hotel where he works, Dexter manages to get close to Jaworski and notices a tattoo. Dexter follows Jaworski to an abandoned construction site which further reveals that Jaworski was a killer and also a thief who has been stealing copper piping and wire to resell for scrap. Dexter takes a look at Jaworski's car but was nearly caught by him, luckily Dexter was able to escape. Dexter decides to break into Jaworski's house to search for evidence which leads him to a website. Dexter returns to his apartment and visits Jaworski's website which reveals it to be a rape site where Jaworski has been uploading snuff videos of him raping his victims. With enough evidence to proof Jaworski's crime, Dexter is given a choice to either to proceed in killing him or call the anonymous tip line to turn over the website to the police so they can arrest Jaworski:
Chapter 5: Robert Marelli
Dexter offers to "help" Doakes on the Marelli case, but Doakes refuses to hand over the case to him, Dexter was able to use Masuka to distract Doakes and manages to get the case notes.