It was written in 1939 and 1940, but after it initially failed to find a publisher, the author withdrew the manuscript from circulation and claimed he had lost it.

[1][2] The Third Policeman is set in rural Ireland and is narrated by a dedicated amateur scholar who studies de Selby, a scientist and philosopher.

Over the next few years, the narrator devotes himself to the study of de Selby's work and leaves Divney to run the family business.

By the time the narrator is thirty, he has written what he believes to be the definitive critical work on de Selby but does not have enough money to have it published.

During a surreal conversation with the apparently dead Mathers, the narrator hears another voice speaking to him which he realises is his soul: "For convenience I called him Joe.

[13]Inside the barracks he meets two of the three policemen, Sergeant Pluck and Policeman MacCruiskeen, who speak largely in non-sequitur and who are entirely obsessed with bicycles.

[14] There he is introduced to various peculiar or irrational concepts, artefacts, and locations, including a contraption that collects sound and converts it to light based on a theory regarding omnium, the fundamental energy of the universe; a vast underground chamber called 'Eternity,' where time stands still, mysterious numbers are devoutly recorded and worried about by the policemen; a box from which anything you desire can be produced; and an intricately carved chest containing a series of identical but smaller chests.

[18]The narrator calls on the help of Finnucane, but his rescue is thwarted by MacCruiskeen riding a bicycle painted an unknown colour which drives those who see it mad.

[21] Disturbed, he enters the house and finally meets the mysterious and reportedly all-powerful third policeman, Fox, who has the face of Mathers.

[23] Elated by the possibilities before him, the narrator leaves Fox's police station and goes home looking forward to seeing Divney once again; on arrival, he finds that while only a few days have passed in his own life, his accomplice is sixteen years older, with a wife and children.

They both enter the police station and are confronted by Sergeant Pluck, who repeats his earlier dialogue and ends the book with a reprise of his original greeting to the narrator: "Is it about a bicycle?"

[31] In a letter to William Saroyan, dated 14 February 1940, O'Nolan explained the strange plot of The Third Policeman: When you get to the end of this book you realize that my hero or main character (he's a heel and a killer) has been dead throughout the book and that all the queer ghastly things which have been happening to him are happening in a sort of hell which he earned for the killing … It is made clear that this sort of thing goes on for ever … When you are writing about the world of the dead – and the damned – where none of the rules and laws (not even the law of gravity) holds good, there is any amount of scope for back-chat and funny cracks.

Anne Clissman, writing in 1975 in the first major study of Flann O'Brien's work, considers the book to be "in many ways a continuation of some of the ideas expressed in At Swim".

[35] Hopper also notes the wide range of intellectual and cultural influences on the book, including John M. Synge's play The Playboy of the Western World, J.K. Huysmans's novel À rebours, Einstein's theory of relativity, the works of J. W. Dunne and Cartesian dualism.

The critic Hugh Kenner, in a 1997 essay entitled "The Fourth Policeman", advanced a hypothesis to explain why O'Nolan had suppressed the manuscript.

The Third Policeman was featured in a 2005 episode of television series Lost with the intent of providing context for the show's complex mythology,[39] with the result that sales of the book in the three weeks following its mention equalled what it had sold in the preceding six years.

[40] John Cooper Clarke's nonsense prose poem, "Ten years in an open necked shirt" contains the line "What with the drink trade on its last legs and the land running fallow for the want of artificial manures",[41] the same line John Divney uses in the book to explain their lack of funds.