Media mogul, Amos Kyne (Robert Warwick), has died and left his empire to his playboy son, Walter (Vincent Price, not yet typecast as a creepy horror movie star). Walter, wanting to change personnel without getting his hands dirty, creates a high-ranking position and makes his top three men compete for it. The catch is that they have to try and solve the sensationalist case of the so-called Lipstick Murderer. Theres Mark Loving (George Sanders), Jon Griffith (Thomas Mitchell), and Harry Kritzner (James Craig), ready to vie for the position. Loving has Mildred (Ida Lupino), a reporter and occasional lover, as an ally; Harry is currently sleeping with Walters wife, Dorothy (Rhonda Fleming), who he hopes can influence his boss; Griffith wants Ed Mobley (Dana Andrews), columnist and Pulitzer Prize winner, on his side, but Ed doesnt want to involve himself in the battle.
However, Eds connections make him useful, and he decides to help Griffith. Eds girlfriend, Nancy (Sally Forrest), is Loving's secretary and is willing to help to find the killer as well at the expense of her own safety.
While the City Sleeps demonstrates the following tropes:
- Answer Cut: As a very drunk Ed rides in a cab to Mildred's place, he murmurs "I wonder what the nice people are doing tonight." Cut to Nancy admiring the flowers Ed sent her.
- Ax-Crazy: The Lipstick Killer (played by John Barrymore Jr.).
- The Bait: Knowing that the Lipstick Killer will fall for the Batman Gambit, Ed uses Nancy as bait because making their engagement public will easily lure the killer after Ed made fun of him on national TV. Ed, of course, has arranged that a plainclothes policeman will follow Nancy everywhere she goes.
- Batman Gambit: How Ed concludes they will catch the killer. Set up an irresistible bait and wait for him to act like he normally would.
- Celebrity Paradox: Across the street from Nancy's apartment is a theatre showing a movie starring Dana Andrews.
- City Noir: The film takes place in New York (but it was actually shot in LA).
- Chalk Outline: Played Straight as we see one for the second murder.
- The Chick: Both Nancy and Mildred play versions of this for a whole floor of just newspaper men.
- Cold Open: The film begins with the Lipstick Murderers first murder.
- Couldn't Find a Pen: The killer writes "Ask Mother" on the victim's wall in lipstick, hence the name.
- Digging Yourself Deeper: When Ed is trying to win back Nancy on the phone (and failing), he makes things worse when he starts to say "I don't want to be happy, I want...". She hangs up on him before he can finish.
- Extra! Extra! Read All About It!: How Griffith announces that hes won the competition: he makes an extra edition announcing that hes found the killer and the newspaper has the exclusive scoop.
- Film Noir: From the classic era, albeit a little grey-ish: it does have a lighter tone than must noirs.
- Freudian Excuse: The killer has serious mommy issues (because he was adopted) and was humiliated as a young kid (someone called him a girl).
- Go Seduce My Archnemesis: Loving sics Mildred on Ed...which Mildred takes to mean that she is now a free agent, and promptly teams up with Griffith.
- Jerk with a Heart of Gold: It's shown in the very last scene that Walter Kyne took Ed's criticism to heart.
- Local Hangout: Dells: where everyone meets up after work and get very, very drunk (in the case of Ed and Mildred).
- The Profiler: Ed does a good job of figuring out the age, habits, and attitudes of the serial killer considering the limited evidence he leaves at the murder scene (he was, at least, a detective before becoming a writer). Ed then broadcasts his profile on his telecast to irritate the killer and make him do something stupid.
- Sexy Secretary: The curvaceous Nancy, Mark's secretary, who falls in love with Ed.
- Sexy Silhouette: The glorious Rhonda Fleming doing stretching exercises on the other side of a translucent screen. Subverted when the camera pans and reveals that Dorothy is actually wearing a bikini.
- Slasher Smile: The Lipstick Killer does this often.
- Sweater Girl: Nancy wears some absurdly tight sweaters.
- Upper-Class Twit: Walter is fairly clueless, but is cunning enough set his underlings up to vie with each other rather than try to upstage him.
- The Vamp: Mildred to Ed, much to Nancys chagrin; Dorothy Kyne as well.
- Villain Opening Scene: Opens with the Lipstick Killer murdering a woman in her apartment.
- "Where Are They Now?" Epilogue: Something of an accelerated case, as it takes place a bare several hours after the penultimate scene, with Nancy reading in a newspaper that various parties have been promoted or Put on a Bus.
- Wrongly Accused: The janitor found at the first murder is suspect number one for the police even if its only for very flimsy circumstantial evidence.