Shade's poem digressively describes many aspects of his life. Canto 1 includes his early encounters with death and glimpses of what he takes to be the supernatural. Canto 2 is about his family and the apparent suicide of his daughter, Hazel Shade. Canto 3 focuses on Shade's search for knowledge about an afterlife, culminating in a "faint hope" in higher powers "playing a game of worlds" as indicated by apparent coincidences. Canto 4 offers details on Shade's daily life and creative process, as well as thoughts on his poetry, which he finds to be a means of somehow understanding the universe.
In Kinbote's editorial contributions he tells three stories intermixed with each other. One is his own story, notably including what he thinks of as his friendship with Shade. After Shade was murdered, Kinbote acquired the manuscript, including some variants, and has taken it upon himself to oversee the poem's publication, telling readers that it lacks only line 1000. Kinbote's second story deals with King Charles II, "The Beloved," the deposed king of Zembla. King Charles escaped imprisonment by Soviet-backed revolutionaries, making use of a secret passage and brave adherents in disguise. Kinbote repeatedly claims that he inspired Shade to write the poem by recounting King Charles's escape to him and that possible allusions to the king, and to Zembla, appear in Shade's poem, especially in rejected drafts. However, no explicit reference to King Charles is to be found in the poem. Kinbote's third story is that of Gradus, an assassin dispatched by the new rulers of Zembla to kill the exiled King Charles. Gradus makes his way from Zembla through Europe and America to New Wye, suffering comic mishaps. In the last note, to the missing line 1000, Kinbote narrates how Gradus killed Shade by mistake.
The reader soon realizes that Kinbote is King Charles, living incognito—or, though Kinbote builds an elaborate picture of Zembla complete with samples of a constructed language, that he is insane and that his identification with King Charles is a delusion, as perhaps all of Zembla is.
Nabokov said in an interview that Kinbote committed suicide after finishing the book. The critic Michael Wood has stated, "This is authorial trespassing, and we don't have to pay attention to it," but Brian Boyd has argued that internal evidence points to Kinbote's suicide. One of Kinbote's annotations to Shade's poem (corresponding to line 493) addresses the subject of suicide at some length.