The story begins with a description of a young mother who feels she is unlucky despite having many advantages. The woman is privileged and attractive, but neither is enough to sustain her happiness. She marries the man she loves, but the love fades away. She has beautiful children, but try as she might, she doesn't feel love for them. She worries about this and reacts by being especially kind yet anxious with her children. Everyone around her thinks she is a wonderful mother, but she and the children both know she does not love them. The family lives in a nice house in a good neighborhood. They have servants and feel they are better than their neighbors, but the mother and her husband do not make enough money to keep up these pretenses. They both have incomes, but the husband’s efforts never amount to much. Regardless, the couple continues living beyond their means, which results in a chronic shortage of money. 

Neither the mother nor her husband can figure out a way to make more money. This causes the mother to feel like a failure, and the constant worry ages her. The situation only gets worse as the children begin to grow up and need to be sent to school. Soon, the anxiety around money becomes so intense that it begins to manifest itself as a whisper coming from the house itself, repeating, "There must be more money! There must be more money!" The need for money is not openly stated by anyone in the family, but the whispers are everywhere and constant, and the children and the dog can hear them too. Inanimate objects like the dolls and the rocking-horse seem to also hear the whispers. 

One day, the boy Paul asks his mother why the family doesn’t have their own car. The mother explains that they are the poor members of the family. Paul asks why and his mother tells him it is because his father has no luck. She explains that luck is what causes a person to have money because if a person is rich, she can lose her money, but if she is lucky, she will always get more. In her answers to Paul’s many questions about luck and money, the mother explains that she may have been a lucky person on her own, but when she got married to her unlucky husband, she stopped being lucky. In response to all of this, Paul proclaims himself lucky because God told him so. 

Paul comes away from the conversation feeling angry and thinks that his mother either doesn’t believe he is lucky or else is not paying attention. Determined to get her attention, Paul begins to search for “luck” within himself. He commands his rocking-horse to take him where luck is and rides it so furiously that his sisters become frightened. Paul continues this strange behavior even as he grows older. His nurse and sisters tell him to stop, but he defiantly continues his search. 

One day, Paul’s mother and his uncle Oscar come into Paul’s room while he is riding the rocking-horse. Paul’s mother anxiously chides him for being too old for the rocking-horse, but Paul pays no attention and continues to ride furiously. Finally, Paul stops, dismounts, and announces that he got where he wanted to go. Uncle Oscar humors Paul good-naturedly, assuming Paul is simply playing make-believe, but Paul is completely serious. In the conversation that follows, Uncle Oscar learns that Paul gives different names to his rocking-horse, including the name of the winning horse of an important race in the real world. Paul’s older sister Joan tells Uncle Oscar that Paul has learned all about horse-racing from Basset, the family gardener who had been Oscar’s batman in the war. Oscar visits Bassett and asks him whether Paul ever bets on the horses, but Bassett is very serious about the matter and won’t say.  

More curious than ever, Uncle Oscar decides to take Paul to the racetrack. On the way there, he questions Paul about the horses. Paul tells his uncle he has been betting on horses in partnership with Bassett and asks Uncle Oscar to keep it a secret. It is also revealed that Paul is very shrewd and careful with his money, always keeping twenty pounds in reserve. Uncle Oscar is astonished at learning all of this and asks Paul for a tip in the upcoming race. At the racetrack, Paul and Uncle Oscar win on Paul’s tip, and Paul explains that he has won fifteen hundred pounds total on horse-racing, which he keeps with Bassett. 

One afternoon sometime later, Uncle Oscar takes Paul and Bassett to the park to discuss becoming partners with them in their horse-race betting. Bassett explains how it started with Paul being curious about Bassett’s gambling and how, after a few initial bets, their luck took a turn for the good. Paul mysteriously tells his uncle that sometimes he is not quite sure of the winner, but when he is, he and Bassett place a heavy bet. Oscar asks to see the fifteen hundred pounds Paul claims to have in Bassett’s care and Bassett produces it. Still finding the whole thing strange, and a little funny, Oscar decides to become a partner in the endeavor. 

In the next big race, Paul is “sure” the winner will be Lively Spark, and they place their bets. When Lively Spark comes in first, Oscar wins 2,000 pounds and Paul wins 10,000. This large sum and the unusual way they got it make Oscar nervous, but Paul assures him there’s nothing to be worried about when he is sure about a horse. When Oscar asks Paul what he plans to do with his money, Paul reveals that he wants to make enough money to get his mother out of debt and stop the house from whispering. Uncle Oscar seems to understand this all too well. He agrees to arrange for Paul’s mother to receive some of Paul’s winnings without her knowing where the money came from. Oscar gives five thousand pounds of Paul’s winnings to the family lawyer, citing an anonymous family benefactor, with instructions to deposit it in his mother’s account in one-thousand-pound installments each year on her birthday.  

To quiet the whispers in the house, which have grown louder than ever, Paul's mother secretly gets a job in town illustrating advertisements for women’s clothing. She does well but makes considerably less than her boss, rendering her more bitter than ever. During breakfast with Paul on the morning of her birthday, his mother reads a letter from the lawyer about the money from an anonymous family member. Paul anxiously watches, anticipating her happiness at the gift. Instead, his mother becomes even colder and says nothing. She later arranges a meeting with the lawyer to ask for all five thousand pounds at once, rather than in yearly installments. Oscar surreptitiously confers with Paul about this, and Paul agrees to let his mother have the full amount. With the windfall, the family buys nicer furniture. They pay for a tutor for Paul and to enroll him at a prestigious school for next fall. But instead of quieting the voices in the house, the money seems to make the voices grow even louder.  

Frightened by the voices and desperate to make more money, Paul’s obsession reaches new heights. Two big races come and go without Paul “knowing” the winner, and Paul becomes even more disturbed. Uncle Oscar tells him to leave it alone, but Paul ignores him. Paul’s mother notices the change in him and encourages him to go to the seaside for a vacation, but Paul insists on staying because of the upcoming Derby race. His mother expresses her disapproval at Paul’s obsession with horse-racing and reveals that her family has always had gambling problems. After she reluctantly allows Paul to stay, it is finally revealed to the reader that Paul’s intuition about the horse-races comes from the rocking-horse he had as a small boy. Paul had the rocking-horse moved from the nursery to his own room years ago and secretly rides it at night until he enters a sort of clairvoyant trance state and learns the name of the winner of an upcoming race. 

Two nights before the Derby, Paul’s mother is at a party when anxiety about Paul overcomes her. She rushes home to check on him and finds Paul in his room, in the dark, frantically riding his rocking-horse. When Paul’s mother flicks on the light, Paul suddenly screams, "It's Malabar!" before falling off the horse and collapsing to the ground sick with a fever. Despite Paul’s illness, Oscar and Bassett bet on Malabar in the Derby. The night after the race, Paul’s health is critical, but Bassett visits his bedside to let him know that Malabar won and that Paul won over 70,000 pounds. Paul excitedly exclaims to his mother that he is lucky after all, but he later dies in the night from his mysterious illness. With Paul lying dead in her arms, Paul’s mother hears Uncle Oscar's voice addressing her as “Hester.” Oscar tells her that though her son is dead, she now has 80,000 pounds, and Paul is probably better off dead than alive in a life where he rides his rocking-horse to find a winner.