The Story of Tom Brennan opens with the Brennan family moving out of their home in Mumbili in the middle of the night. As the first chapter begins, we learn that the narrator, Tom, and his family have all moved into his grandmother's house as the school year starts. As Tom settles into his new life and returns to playing rugby, we learn through a series of flashbacks that something serious has happened to make them leave their hometown, something to do with his brother, Daniel, who is in prison. Over the next weeks, while Tom and Kylie start going to school in the present, we discover that Daniel crashed his car while driving drunk after having an argument with their cousin, Fin, over Daniel's girlfriend.
Tom is struggling to fit in but meets people like the Tulakes—Jonny and his sister, Chrissy—who make things better. When Tom goes to visit Fin (who was paralyzed as a result of the accident) with his uncle Brendan, they're kind enough to give him a wool booty for Fin, even though they think it's for Tom's grandfather. The visit with Fin, however, is stressful for Tom and causes him to remember the worst details of the accident. Since visiting Fin is stressful and there's not enough space for him to visit Daniel, he spends most of his weekends alone while everyone in his family is out of the house. Alone, Tom remembers why Sunday mornings are so difficult for him by reflecting on how the morning after the accident was particularly hard for everyone.
Tom tries out for the football team at his new school, St. Benedict's (Bennie's), and makes the firsts, although he's not very excited since he thinks that the team is awful. In the days before he and Brendan go to see Daniel for the first time in a while, Tom reflects on how much his life has changed and again flashes back, this time to the days before the sentencing. At the prison, they quickly realize that Daniel is struggling, and Daniel moves to the Westleigh Peer Support facility a week later. Tom also begins to run in the mornings with Brendan, and Aunty Kath, Fin's mother, comes to visit. There is a fight where Aunty Kath confronts Tom's mother, who has been going through a deep depression, about not being involved enough in her younger children's lives after Daniel was sent to prison. Although Aunty Kath's criticism isn't completely fair, it still manages to get Tom's mom out of the house.
Some weeks later, Tom and his sister, Kylie, get into a fight after Kylie tells her public speaking class about Daniel's accident and how the town harassed them in the aftermath. Coghill proves to be different, however, and they end up receiving sympathy from their new community. Brendan and Tom go to visit Daniel in the crisis centre, and it appears that he's doing better. Kylie and Tom remain estranged until the night before Fin's birthday when Kylie goes into his room and apologizes. Tom in turn admits that the truth had to come out sooner or later. Fin's birthday goes somewhat smoothly until the family returns to Coghill to find out that Daniel has regressed again. Tom's parents go off to attend to that problem while Tom continues with practice. After Daniel makes enough progress, Tom's dad is able to accompany Tom and his team to their footy camp. Although Tom still thinks that the team is not as technically good as his old team, his dad pushes him to appreciate the way that the boys from Bennie's truly love playing football, something that was lost for their team in Mumbili.
After Tom visits Daniel alone, he realizes that they have grown apart in the way that they see rugby. Tom's mother apologizes for not being mentally present. Chrissy and Jonny, who have been hanging out with Brendan and Tom throughout the book (Jonny being Brendan's boyfriend), invite them to dinner after a match against their rival school. Chrissy convinces Tom to take Brendan's suggestion for what to do over Christmas: go to Nepal. Tom comes home that night to find Kylie has cut her hair. When he asks why, she tells him that she is struggling to work through her guilt about the accident. She feels responsible for the accident because she set Fin and Claire, Daniel's girlfriend, up with each other, and Claire was the subject of the fight between Fin and Daniel. Tom, however, reassures her that it was neither of their faults, and there was nothing that they could have done.
On one of their morning runs, Brendan introduces Tom to his special secret watering hole and Tom suggests that they should build a chicken coop for Gran, with whom he's gotten much closer, for her birthday. The team prepares for the match against St. John's, Tom's old school, and his new teammates support Tom all the way through. Although they lose the game, they're proud of their performance in the end. One of the people in the audience, however, yells out something about Brennans being killers, which throws Tom off. As he's stalking off the field, Chrissy comes up and they drive off together. Once they stop, Tom finally opens up, telling Chrissy about his situation. Tom kisses her, and they start dating.
The family helps Fin put together the house he'll be living in once he's out of recovery, and Tom has a party for his eighteenth birthday soon after Gran's party, where he gives her the completed chicken coop. Gran buys him tickets to Nepal in exchange. As the book closes, Tom takes Chrissy back to the watering hole and has sex with her.