A number of Allegro's later books, including The Sacred Mushroom and the Cross, brought him both popular fame and notoriety, and also complicated his career.

After the war he began training for the Methodist ministry, but found that he was more interested in Hebrew and Greek, so he went to study at Manchester University with fees paid by government grant due to his military service.

[5][6][7] It was on Allegro's recommendation in 1955 that the Copper Scroll was sent by the Jordanian government to Manchester University in order for it to be cut into sections, allowing the text to be read.

He was present during the cutting process in 1956 and later made a preliminary transcription of the text, which he soon translated, sending copies of his work back to Gerald Lankester Harding in Jordan.

[17] Allegro was entrusted with the publication of 4Q158–4Q186, a collection of fragments which mainly contained exemplars of a unique kind of commentary on biblical works known as pesharim.

He told de Vaux that he could have his share of the texts ready in 1960, but due to hold ups had to wait until 1968 for his volume, Discoveries in the Judaean Desert of Jordan V: 4Q158–4Q186, to be published.

[21] As early as 1956 Allegro held controversial views regarding the content of the scrolls, stating in a letter to de Vaux, "It's a pity that you and your friends cannot conceive of anything written about Christianity without trying to grind some ecclesiastical or non-ecclesiastical axe."

[18] It was during his stay in Theology that he wrote his controversial book, The Sacred Mushroom and the Cross, whose subtitle was "A Study of the Nature and Origins of Christianity within the Fertility Cults of the Ancient Near East".

[28] Allegro argued that Jesus in the Gospels was in fact a code for a type of hallucinogen, the Amanita muscaria, and that Christianity was the product of an ancient "sex-and-mushroom" cult.

[29][30] Critical reaction was swift and harsh: fourteen British scholars (including Allegro's mentor at Oxford, Godfrey Driver) denounced it.

Jenkins called the Sacred Mushroom and the Cross "possibly the single most ludicrous book on Jesus scholarship by a qualified academic".

[36] Among Allegro's works are the following: His scholarly journal articles include: An undated play 'The Lively Oracles' (with Roy Plomley).