He had long been part of the critical audience for his father's fiction, first as a child listening to tales of Bilbo Baggins, and then as a teenager and young adult offering much feedback on The Lord of the Rings during its 15-year gestation. He had the task of interpreting his father's sometimes self-contradictory maps of Middle-earth in order to produce the versions used in the books, and he re-drew the main map in the late 1970s to clarify the lettering and correct some errors and omissions.
In 2001, he received some attention for his stance toward The Lord of the Rings film trilogy directed by Peter Jackson. He expressed doubts over the viability of a film interpretation that retained the essence of the work, but stressed that this was just his opinion.
Christopher Tolkien currently lives in France with his second wife, Baillie Tolkien (born Baillie Klass), who edited J. R. R.'s The Father Christmas Letters for posthumous publication. They have two children, Adam Reuel Tolkien and Rachel Clare Reuel Tolkien. His elder son by his first marriage to Faith Faulconbridge, Simon Mario Reuel Tolkien, is a barrister and novelist.
After his father's death, Christopher Tolkien embarked on organizing the masses of his father's notes, some of them written on odd scraps of paper a half-century earlier. Much of the material was handwritten; frequently a fair draft was written over a half-erased first draft, and names of characters routinely changed between the beginning and end of the same draft. Deciphering this was an arduous task, and perhaps only someone with personal experience of J. R. R. Tolkien and the evolution of his stories could have made any sense of it. Christopher Tolkien has admitted to having to occasionally guess at what his father intended.
Working with Guy Gavriel Kay, he was able to complete The Silmarillion, which was published in 1977. The Silmarillion was edited by Christopher Tolkien, who had to make some difficult editorial decisions when deciding how to present the material, and both Christopher Tolkien himself, and others have criticised some of these decisions. The Silmarillion was followed by Unfinished Tales in 1980, and the twelve-volume The History of Middle-earth between 1983 and 1996.
In April 2007 Christopher published a "new" book by his father, The Children of Húrin, which Tolkien had written between 1951-57 and brought to a relatively completed stage before he abandoned it. This was one of the elder Tolkien's earliest stories, its first version dating back to 1918; several versions of the story are published in The Silmarillion, Unfinished Tales and The History of Middle-earth. The Children of Húrin is a synthesis of these and other sources.
Tolkien is currently in a legal case against New Line Cinema, who he claims owes his family £80m.