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Born in Groningen as the son of Dirk Huizinga, a professor of physiology, and Jacoba Tonkens, who died two years after his birth, he started out as a student of Indo-Germanic languages, earning his degree in 1895. He then studied comparative linguistics, gaining a good command of Sanskrit. He wrote his doctoral thesis on the role of the jester in Indian drama in 1897.
It was not until 1902 that his interest turned towards medieval and Renaissance history. He continued teaching as an Orientalist until he became a Professor of General and Dutch History at Groningen University in 1905. In 1915, he was made Professor of General History at Leiden University, a post he held until 1942. Huizinga was guest at the 1937 wedding of Juliana of the Netherlands with Prince Bernhard of Lippe-Biesterfeld. 
In 1942, he spoke critically of his country's German occupiers, comments that were consistent with his writings about Fascism in the 1930s. From then until his death in 1945, he was held in detention by the Nazis. He died in De Steeg in Gelderland, near Arnhem, just a few weeks before Nazi rule ended, and he lies buried in the graveyard of the Reformed Church at 6 Haarlemmerstraatweg in Oegstgeest.
Huizinga had an aesthetic approach to history, where art and spectacle played an important part. His most famous work is The Autumn of the Middle Ages (a.k.a. The Waning of the Middle Ages) (1919). He here reinterpreted the later Middle Ages as a period of pessimism and decadence rather than rebirth.
Worthy of mentioning are also Erasmus (1924) and Homo Ludens (1938). In the latter book he discussed the possibility that play is the primary formative element in human culture. Huizinga also published books on American history and Dutch history in the 17th century.
Alarmed by the rise of National Socialism in Germany, Huizinga wrote several works of cultural criticism. Many similarities can be noted between his analysis and that of contemporary critics such as Ortega y Gasset and Oswald Spengler. Huizinga argued that the spirit of technical and mechanical organisation had replaced spontaneous and organic order in cultural as well as political life.
Huizinga's son Leonhard Huizinga became a well-known writer in the Netherlands, especially renowned for his series of tongue-in-cheek fiction novels on the Dutch aristocratic twins Adrian and Oliver ("Adriaan en Olivier").
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