By March 1518 Alfonso d'Este had grown exasperated with how slowly his camerino project was moving and commissioned Titian directly to paint The Worship of Venus, giving him six months to complete it. To speed the process, Alfonso sent Titian a drawing Fra Bartolommeo had already made for the same subject, a copy of the Philostratus text describing it, detailed instructions on its content, and the canvas and stretcher it was to be painted on^[1]. Titian replied on 1 April, only ten days after the unveiling of his Assumption of the Virgin in the Frari, flattering the duke's conception of the scheme while quietly warning that six months might not be enough time to bring the picture to the finish he wanted^[1].

Titian based the painting on Philostratus's description of an imagined gallery picture showing cupids at play in a garden sacred to Venus, gathering apples as tokens of love. He positioned a statue of Venus, of a Praxitelean type related to figures such as the Townley Venus, off to one side, leaving the centre of the canvas open for a crowd of infant loves kissing, fondling, leaping and playing rhythmic games, some shooting arrows at a rival faction who answer by throwing apples back^[2]. The device of moving the central statue aside recurs elsewhere in Titian's work of these years, including his roughly contemporary reworking of the sacra conversazione for the Pesaro family in the Frari, where he shifted the Virgin to one side of the composition in a similarly unconventional way^[1].

Alfonso had originally hoped to fill his camerino with bacchanals by the leading masters of Venice, Rome and Florence, an ambition shaped by his sister Isabella d'Este's own studiolo in Mantua, for which she had once tried unsuccessfully to enlist Giovanni Bellini^[5]. That scheme collapsed when Fra Bartolommeo and then Raphael died before completing their contributions, in 1517 and 1520, and both commissions passed to Titian, who delivered the Worship of Venus, based on Fra Bartolommeo's earlier sketch, in 1519^[4]. Over the following years Titian added The Bacchanal of the Andrians and Bacchus and Ariadne to the room, while the court painter Dosso Dossi supplied a further bacchanal and a painted ceiling and frieze to complete the decoration^[4].