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The origins of Venus and Cupid with the Honeycomb are unknown. However, as many historians have demonstrated, Cranach is thought to have applied his first paintbrush strokes in XVI century, in Wittemburg, a small town in northern Germany.

According to Kristina Herrmann Fiore, the artwork was eventually given to Cardinal Scipione Borghese as a gift by Paduan jurist Alvise Corradini. Nevertheless, there is still a great deal of mystery surrounding what followed after the picture was entrusted to the cardinbal. However, it is known that the picture was framed by the carpenter Annibale Corradini in these exact years, around 1611, thanks to the recording of an invoce.

Venus and Cupid with the Honeycomb made its initial appearance in an art gallery alongside Venus and two Cupids in the early XVII century. The picture eventually disappeared due to curious transfers from one institution to another, and it wasn't found again until 1883 when it resurfaced in some records that identified the painting's real creator.