In 1244, the Ayyubids allowed the Khwarazmians, whose empire had been destroyed by the Mongols in 1231, to attack the city. The Templars began fortifying the city of Jerusalem in 1244 when the Khwarezmian invasion occurred, a force summoned by as-Salih Ayyub, the sultan of Egypt. They seized Tiberias, Safed and Tripoli and began the Siege of Jerusalem on 15 July 1244. Because of the agreement between Frederick II and al-Kamil, the walls were inadequately fortified and unable to withstand the attack. The patriarch of Jerusalem Robert of Nantes and the leaders of the Templars and Hospitallers came to support the city's inhabitants and initially repelled the attackers. The imperial Castellan and the Grand Commander of the Hospital lost their lives in the battle, but no help from the Franks was coming.

The city fell rapidly. The Khwarazmians plundered the Armenian Quarter, where they decimated the Christian population, and drove out the Jews. In addition, they sacked the tombs of kings of Jerusalem in the Church of the Holy Sepulchre and dug out their bones, in which the tombs of Baldwin I and Godfrey of Bouillon became cenotaphs. On 23 August, the Tower of David surrendered to the Khwarazmian forces, some 6,000 Christian men, women and children marched out of Jerusalem. The Knights Hospitaller and Templars moved their headquarters to the city of Acre.