The model introduced by Giorgione in his Sleeping Venus had a prototype in a woodcut of a sleeping nymph propagated in Francesco Collonna's romance "Hypnerotomachia Poliphili" published in 1499, which itself derived from an ancient statue depicting sleeping Ariadne or Cleopatra. Images of Venus and Cupid in the landscape were a favorite motif of the golden age of Venetian painting, especially in the circle of Giorgione and Titian. The artist studied briefly with Titian from whom he acquired the concept of reclining nude, possibly poetically inspired and with epithalamic meaning. Bordone become one of the most successful followers in the type known as Titianesque nude.
According to Keith Christiansen the ancient marriage poems known as epithalamia were reflected in visual arts in depiction of Amor urging his mother to raise from her bower and give her blessing to the brides. The goddess is holding a myrtle wreath. The plant is specifically associated with matrimony as stressed in Catullus poetry freely translated in 1538 by Venetian author Ludovico Dolce. Such paintings were usually commissioned as a wedding gift to ensure happiness and fertility of marriage. The Arcadian landscape was frequently linked with the subject of love in the mid 16th century. Venus in the foreground seems to be a natural inhabitant of Arcadia - the embodiment of the secrets of nature. Naked Venus was also conceived as a personification of the innate beauty - pulchritudo innata, as opposed to artificial charms - ornamentum.
The painting is softly modelled, harmonious and full of scattered light and vivid colors. It was possibly created for Francis, second duke of Guise for the chamber shared by the duke and his wife Anna d'Este of Ferrara. This provenance would also arrange later history of the painting in geographically logical order, however the date of creation should be moved to the years 1558-59, when according to Vasari the artist painted uno da camera di Venere e Cupido (one of Venus and Cupid for his bedroom), during his stay in France. In first half of the 17th century the picture came into possession of a renowned painter Sir Peter Lely in London, and in 1682 it was purchased at an auction of Lely's collection by Anthony Gray, 11th Earl of Kent for £105. Later it was in the collection of Ayerst Hooker Buttery, to be acquired by Karl Haberstock from Otto Neumann in 1928, and then by Adolf Hitler from Haberstock in 1936. The painting adorned Führer's residence at Berghof near Berchtesgaden. In postwar chaos the painting was mistakenly identifed as one of the paintings looted by the Germans from the National Museum in Warsaw. Since such property evidently cannot be reclaimed it was not returned to Germany and included in the museum's collection under the number 187158.