After publication, Juster sent a copy of the book to the Ford Foundation, with an explanation of how the projected book on cities had transformed into The Phantom Tollbooth. He never heard back from them, and learned years later that they were delighted by the turn of events. With the book having become an unexpected hit, Juster found himself answering letters from young readers, and a few parents. He found that children understood the wordplay at different ages, and heard from the occasional college student as well. Some students wrote a second time after a gap of years "and they'll talk to me about a whole different book, normally. But now they've got a lot more of the words right. A lot more of the fun kind of crazy references". He learned too that readers were capable of more than he had intended, as in the case of the letter sent by the Mathemagician to King Azaz. Composed entirely of numbers, some readers assumed it was a code and set about breaking it, only to appeal to Juster for help when they were not successful. The numbers were not intended to have any meaning, and were meant to convey that the Mathemagician's letter could not have been understood by Azaz or his advisers.
And, in the very room in which he sat, there were books that could take you anywhere, and things to invent, and make, and build, and break, and all the puzzle and excitement of everything he didn't know—music to play, songs to sing, and worlds to imagine and then someday make real. His thoughts darted eagerly about as everything looked new—and worth trying.The Phantom Tollbooth (home again) 
As the book became acclaimed as a modern classic, it began to be used in the classroom, and Juster corresponded with some teachers. After the book's readers attained adulthood, they wrote of its influence on them. Novelist Cathleen Schine recalled, "it was as if someone had turned on the lights. The concepts of irony, of double entendre, of words as play, of the pleasure and inevitability of intellectual absurdity, were suddenly accessible to me. They made sense to me in an extremely personal way." British fantasy writer Diana Wynne Jones read her copy so often it fell apart: "it didn't occur to us that it might be about something. It struck us as a little like The Wizard of Oz, only better." One reader, signing himself "Milo", wrote to Rolling Stone in 1970, "If you want to get freaked out of your undernourished head, pick up The Phantom Tollbooth, by Norton Juster. They tell you it's a kids' book, but take my word for it, no one who reads it is ever the same. No hype."
The book continued to garner positive reviews and comments. In 1998, Amanda Foreman wrote for The Sunday Times of London, "I want to shout about The Phantom from the rooftops. I want to stand in Waterloo and press copies into people's hands. This is a book that should be in every home. ... Whether you are 8 or 88 Juster's mixture of allegorical wisdom and logical whimsy will take you on a journey of the spirit. The Phantom is a mappa mundi of our hearts, proving once again that in laughter and simplicity lies the truth of life". In a 2011 article written for the book's fiftieth anniversary, Adam Gopnik wrote, "The book is made magical by Juster's and Feiffer's gift for transforming abstract philosophical ideas into unforgettable images."
The book has been translated into many foreign languages, including Chinese, Croatian, Japanese, Korean, Russian, Thai, Turkish and three different Spanish editions: one for Spain, one for Latin America, and one for Spanish speakers in the United States. Juster states that he does not know if the wordplay of the original carries through to the translated works. In 1970, Chuck Jones made it into a musical film of the same name, with Milo's room in live action, and animation beyond the tollbooth. Juster dislikes the film, describing it as "drivel". In February 2010, director Gary Ross began development of a remake of The Phantom Tollbooth, with the first draft of the script written by Alex Tse. As of August 2016, the remake has moved to TriStar Pictures, with Michael Vukadinovich writing the adaption.
In 2011, The Annotated Phantom Tollbooth was published, which includes sketches and copies of Juster's handwritten drafts and word lists, Feiffer's early drawings, and an introduction and annotations by Leonard S. Marcus. A fiftieth anniversary edition was also published, with appreciations by Maurice Sendak, Michael Chabon and Philip Pullman. More than three million copies have been sold of the original book in the U.S. alone. It has been adapted into a small-scale opera with music by Arnold Black, and book by Juster and Sheldon Harnick, produced by Opera Delaware in 1995. It was then revamped into a musical that had its debut to strong reviews at the Kennedy Center in Washington, D.C. and then made a national tour.
The Phantom Tollbooth remains acknowledged as a classic of children's literature. Based on a 2007 online poll, the U.S. National Education Association named it one of "Teachers' Top 100 Books for Children". In 2012, it was ranked number 21 among all-time children's novels in a survey published by School Library Journal.
Juster feels that his book still has relevance today, although children's lives have changed since 1961:
When I grew up I still felt like that puzzled kid—disconnected, disinterested and confused. There was no rhyme or reason in his life. My thoughts focused on him, and I began writing about his childhood, which was really mine ... Today's world of texting and tweeting is quite a different place, but children are still the same as they've always been. They still get bored and confused, and still struggle to figure out the important questions of life. Well, one thing has changed: As many states eliminate tolls on highways, some children may never encounter a real tollbooth. Luckily there are other routes to the Lands Beyond. And it is possible to seek them, and fun to try.