The painting depicts a Biblical scene, specifically Revelation 3:20, in which Jesus says "Behold, I stand at the door and knock". Hunt painted the door as ancient and overgrown with no external handle, in order to represent the problems of a closed mind.

The work took until 1853 to finish, and during this time he was also painting a smaller version later acquired by Manchester Art Gallery. Although the precise year of Hunt beginning work on The Light of the World is unknown, a date of c. 1850 is generally accepted.

Some sources claim that Hunt aided his representation of the pre-dawn setting by painting it after dark in a hut on a Surrey farm; others maintain that his location was the Oxford University Press garden. The distinctive lighting may have been informed by a journey to Bethlehem Hunt performed at about this time.

Upon the completion of The Light of the World, it was shown at the 1854 Royal Academy exhibition, and was very popular: Arthur Sullivan's oratorio of the same name is inspired by it.

Almost twenty years later, a notable patron of Pre-Raphaelite artists, Thomas Combe, presented the painting to Keble College at Oxford University.

There was some controversy about this, since Combe wanted the work to hang in the chapel that was imminent, but William Butterfield, the building's architect, objected. It took until the early 1890s for the row to be resolved, with the construction of a new side chapel.

Hunt was not pleased by Keble's decision to charge for admission to see his painting, so in 1900 he began work on a new, life-size version. Hunt was now elderly and in poor health, so asked for assistance from Edward Robert Hughes.

On the new work's completion four years later, it was bought by a wealthy shipowner, who took it on a hugely successful world tour. In 1908, the painting returned to England to be dedicated in its new home, St Paul's Cathedral. Hunt himself lived to see this, but not much longer: he died two years later, to be buried in St Paul's.