San Francisco debutante Nicki Collins goes to visit her aunt in New York. Her father's employee, Haskell, is to meet her and facilitate her stay. Before reaching Grand Central, Nicki's train makes a brief stop and she looks up from reading a mystery by novelist Wayne Morgan—and witnesses a murder in a nearby building.
Upon arrival, she slips away from Haskell and goes to the police, but the desk sergeant, seeing the novel in her hand, assumes she imagined the crime. She decides that Wayne Morgan must be able to solve a murder, finds him, and pesters him to get involved. Following Morgan and his fiancee into a theater, she sees a newsreel about the "accidental" death of shipping magnate Josiah Waring—and recognizes him as the murder victim.
Unable to find the crime scene, Nicki sneaks onto the grounds of Waring's mansion. She is mistaken for Margo Martin, who was expected but has not come. Waring's will is read by his lawyer, Wiggam: Waring's nephews Arnold and Jonathan are not surprised to receive a token $1 inheritance, while the bulk of the estate goes to Margo Martin—his trophy fiancee, a singer at a nightclub he owns. Nicki snoops around the house and takes away a pair of bloody slippers that disprove the story of an accident. Two conspirators in the murder try but fail to stop her: Saunders, who turns out to be the nightclub's manager and another heir, and the chauffeur Danny.
Back with Haskell, Nicki makes another attempt to involve Morgan, phoning him and pretending a man is there attacking her—not realizing that Danny is there and is about to. Before he can, she makes another call, to her father. While she is singing to him, Danny spots the slippers and departs, separately attacking Haskell and Morgan. (Nicki assumes they mistakenly attacked each other.)
For various reasons, everyone goes to the nightclub. Nicki speaks to Margo and becomes suspicious. She locks Margo in a closet, goes on stage, and sings in her place. When freed, Margo tells Saunders she was never interested in the plot and stalks off; she is later murdered.
Arnold and Jonathan make romantic overtures to Nicki, but Saunders has her called backstage. He and Danny admit their involvement in the murder and threaten her, but Morgan breaks into the room and Nicki takes the slippers back. A series of backstage fights follows. Nicki escapes back to the stage and sings again. Morgan learns that one of the people she is sitting with—Arnold, Jonathan, and Wiggam—must be the murderer and manages to warn her. Meanwhile, Morgan's fiancee, thinking he is two-timing her with Nicki, dumps him.
Danny shoots Saunders. Nicki and Morgan leave with the slippers, but are arrested in the morning based on false information from Danny. Nicki tries to present the slippers, but Morgan's valet has them—and proudly shows how clean they now are.
Arnold, Jonathan, and Haskell all arrive at the jail to pay Nicki's bail. Arnold says the Warings would like to meet her and drives her to their company's offices, but nobody is there. They talk about the case and he admits that he had motive, but so did Jonathan, Wiggam, and especially Saunders. Nicki, frightened, manages to get away from him.
Finding Jonathan in the building, she tells him that Arnold is the murderer. They hide in a room—and it is the scene of the crime she saw from the train. Jonathan is the murderer. He confesses braggingly: next he will kill her, frame Arnold, and kill Arnold supposedly while defending Nicki.
Arnold slips into the room and grabs Jonathan's gun, but then Morgan arrives and mistakes the situation, and Jonathan gets it back. As Morgan tries unconvincingly to tell Jonathan that the police will be coming, they do.
In the final scene, Nicki and Wayne Morgan are newlyweds on a train. She is enjoying his newest book so much she tells the porter not to make up their beds until she finishes reading, and Morgan promptly tells her how it ends.Deanna Durbin as Nicki Collins
Ralph Bellamy as Jonathan Waring
David Bruce as Wayne Morgan
George Coulouris as Mr. Saunders, Circus Club Manager
Allen Jenkins as Danny
Dan Duryea as Arnold Waring
Edward Everett Horton as Mr. Haskell
Jacqueline deWit as Miss Fletcher
Patricia Morison as Joyce Williams
Elizabeth Patterson as Aunt Charlotte Waring
Maria Palmer as Margo Martin
Samuel S. Hinds as Mr. Wiggam
William Frawley as Desk Sgt. Brennan
Thurston Hall as Josiah Waring (uncredited)
Kathleen O'Malley as Photographer
"Silent Night" (Joseph Mohr, Franz Gruber, John Freeman Young)
"Give Me a Little Kiss" (Roy Turk, Jack Smith, Maceo Pinkard)
"Night and Day" (Cole Porter)
In 1957, Agatha Christie's 4.50 from Paddington was published, using a story markedly similar to that of Lady on a Train. In 1990, Charteris's story was adapted for the pilot episode of the television series Over My Dead Body.
The scenario of a lady witnessing a murder from a train was used as the basis for the Return of the Saint episode "Signal Stop"—the character of Simon Templar having been created by Lady on a Train writer Leslie Charteris. The executive producer of Return of the Saint, Robert S Baker, said that Leslie Charteris was surprised on reading the "Signal Stop" script, noting its similarity with Lady on a Train. It is not known whether "Signal Stop" writer John Kruse had seen the film prior to writing the episode.1946 Academy Award Nomination for Best Sound (Bernard B. Brown)