[1] The show's writers convened during February and March 2009 to brainstorm ideas for the fourth season, and filming was scheduled to begin in June 2009.

[2] In May 2009, Showtime announced that John Lithgow would guest star in all 12 episodes as Miami's latest and deadliest serial killer, and Keith Carradine would return as Lundy.

[3] The fourth season focuses on Dexter attempting to find his way to balance his family life, the birth of his son, and his "extra-curricular" activities.

Rita becomes upset that Dexter appears to be lying to her, including keeping his old waterfront condo where he has stashed his blood drop trophies, and their marriage goes through troubling times.

As the police investigate a series of small-time crimes and killings in the so-called "Vacation Murders" with the help of investigative journalist Christine Hill, retired FBI Special Agent Frank Lundy returns to Miami; Debra initially worries he has come back to get closer to her, but he later reveals that he is following a case that the FBI refused to handle.

Dexter learns of Lundy's analysis, steals his records, and uses his own skills to sneak into the building and catch sight of the Trinity Killer in the act of dispatching his third victim.

Dexter follows the killer to his home, and is very surprised to learn that he is Arthur Mitchell: husband and father, deacon at a local church, and leader of the "Four Walls One Heart" homebuilding charity organization.

Using the alias "Kyle Butler", Dexter joins Arthur's church, befriends him, and learns from him how to improve his own relationship with Rita and his family, giving over his condo to Debra while transferring his killing implements into a shed behind their house.

This is where he, at age ten, saw his older sister die after he inadvertently surprised her in the bathroom; she fell through the glass shower door and severed her femoral artery, killing her almost immediately.

Dexter goes back to find that Lundy has missed this part of Arthur's pattern: each Trinity series was preceded, five days before, by the abduction of a ten-year-old boy – and since the bodies were never found, they were not recorded as killings.

Dexter arranges a getaway for Rita and his children to the Florida Keys as a means to protect them from Arthur, promising to meet them later in the day.

Third season executive producers John Goldwyn, Sara Colleton, Clyde Phillips and Charles H. Eglee all returned to their roles.