In early 1856 Rossetti was commissioned by John P. Seddon, a friend of John Ruskin and the architect responsible for the restoration of Llandaff Cathedral, Wales, to Paint an altarpiece for £400. Rossetti described the work, which heralded his move back to Painting in oils, as 'a big thing which I shall go into with a howl of delight'.

In painting the only Pre-Raphaelite work that related directly to their Italian predecessors- specifically Veronese's Adoration of the Magi of 1573, Rossetti used the traditional triptych composition with a central nativity scene. Tintoretto's Nativity of 1581 was possibly a source of inspiration, as well as his Annunciation of 1583-87, although Rossetti explained that:
'The centerpiece is not a literal reading of the event of the Nativity, but rather a condensed symbol of it.'

The work was first executed in watercolor in 1856, and there is a vast difference in size, technique, style and composition in the final oil version completed eight years later. The figures in the watercolor were in Rossetti's medieval style in contrast to the figures in the oil painting, all of whom are more monumental and with a more developed musculature. The semi-nude David in the left Panel is almost classical in his contrapposto pose, his body having been modeled by Timothy Hughes, Fanny Cornforth's husband, and the head by William Morris.

Swinburne sat for the king and Burne-Jones for the shepherd, while Arthur Hughes's daughter Agnes modeled for the child. The Virgin's body was based upon Fanny Cornforth; her head was originally copied from Ruth Herbert but was changed to depict Jane Morris in 1861.

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