Christopher Tolkien was born in Leeds, England, the third and youngest son of John Ronald Reuel Tolkien. He was educated at the Dragon School in Oxford and then at the Oratory School. He was commissioned into the Royal Air Force in March 1945 and briefly served as a pilot, reaching the rank of Flying Officer, after which he read English at Oxford University.

He had long been part of the critical audience for his father's fiction, first as a child listening to tales of Bilbo Baggins (which were published as The Hobbit), 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.

He published Saga of King Heidrek the Wise: Translated from the Icelandic with Introduction, Notes and Appendices by Christopher Tolkien in 1960. Later, Tolkien followed in his father's footsteps, becoming a lecturer and tutor in English Language at New College, Oxford, from 1964 to 1975.

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 (née Klass), who edited J. R. R. Tolkien's The Father Christmas Letters for posthumous publication. They have two children, Adam Reuel Tolkien and Rachel Clare Reuel Tolkien. Simon Mario Reuel Tolkien, his son by his first marriage, to Faith Faulconbridge, is a barrister and novelist.

J. R. R. Tolkien wrote a great deal of material connected to the Middle-earth mythos that was not published in his lifetime. Although he had originally intended to publish The Silmarillion along with The Lord of the Rings, and parts of it were in a finished state, he died in 1973 with the project unfinished.

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 occasionally guessed at what his father had intended.

In the years following his father's death in 1973 Christopher Tolkien was able to produce an edition of The Silmarillion for publication in 1977; his assistant for part of this work was the young Guy Gavriel Kay, who would later become a noted fantasy author. Christopher Tolkien had to make some difficult editorial decisions in presenting his father's material, and both he and others have criticized some of these decisions. The Silmarillion was followed by Unfinished Tales in 1980 and The History of Middle-earth in twelve volumes between 1983 and 1996; between HME and UT most of the original source-texts from which the 1977 Silmarillion was constructed have been made public.

In April 2007 Christopher Tolkien published The Children of Húrin, whose story his father had brought to a relatively complete stage between 1951 and 1957 before abandoning it. This was one of J. R. R. 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.

In January 2009 HarperCollins announced the forthcoming publication of another J. R. R. Tolkien work edited by Christopher Tolkien: The Legend of Sigurd and Gudrún, a verse retelling of the Norse Völsung cycle. The work was published in May of the same year.

In 2008 Christopher Tolkien commenced legal proceedings against New Line Cinema, which he claimed owed his family £80 million in unpaid royalties. In September 2009, he and New Line reached an undisclosed settlement, and he has withdrawn his legal objection to The Hobbit film.