An exhibition at the Victoria and Albert Museum in London focuses on the legacy of the painting created in Renaissance Italy around 1485 through fashion, photography and the visual arts more broadly.
A grand tour organised by Italian dictator Benito Mussolini in the late 1930s helped to forge the global reputation of the work.
Co-curator Ana Debenedetti said part of its success is in the main subject: a woman with long blonde hair that fits the Western ideal of beauty.
"She fits the image of perfect beauty celebrated since the Middle Ages in poetry, literature and which was embedded in our imagination: the Western woman, blonde, with a pale complexion and a large forehead, blue eyes and a proud bearing," she told AFP.
The Venus is found on everything from the 1993 spring summer collection of Italian fashion house Dolce & Gabbana, to a 2014 video game by Japan's Tomoko Nagao where she is seen floating over Italian pasta.
Brazil's Vik Muniz depicted her in 2007 surrounded by computer detritus, while China's Yin Xin reimagined her with typically Asian features.
Forgotten for four centuries
The exhibition traces how Botticelli, though held in high esteem during his lifetime, was forgotten after his death in 1510 as his fame was supplanted by Renaissance masters Michelangelo and Raphael.
His works are also likely to have fallen foul of a new taste for modesty advocated by the preacher Girolamo Savonarola, who rose to power in Florence.
"His art fell into oblivion and was considered archaic," said Debenedetti, noting that the artistic hub of Italy also shifted from Florence to Rome.
It took four centuries for Botticelli's reputation to be restored.
In the 19th century "we rediscovered works that had remained for centuries in palaces, homes and convents, not accessible to the public," Debenedetti said.
Before the "Birth of Venus" became more widely known, it was Botticelli's "Allegory of Spring" that won hearts and minds of that era.
The painting inspired among others French composer Claude Debussy's orchestral piece "Spring", American dancer Isadora Duncan's performances and Italian artist Attilio Formilli for a famous poster for a flower festival in Florence in 1896.
On show from Saturday until July 3, the exhibition takes up three large rooms, with the final one reserved for around 50 of Botticelli's own works including several Virgin Marys and portraits of young men and women from Florence's bourgeoisie.
As for the "Allegory of Spring" and "Birth of Venus" themselves, art fans will have to travel to the Uffizi Gallery in Florence to admire the originals.