Princess Reema bint Bandar Al Saud, a daughter of the kingdom's longtime ambassador to Washington Bandar bin Sultan Al Saud, faces a stark challenge in improving the image of Saudi Arabia in the US.
The princess will take over from Prince Khalid bin Salman al-Saud amid deteriorating ties with the United States after the death of Saudi dissident journalist Jamal Khashoggi in October previous year.
The reshuffle comes as Saudi Arabia seeks to quell an worldwide outcry over Khashoggi's murder last October in the Saudi consulate in Istanbul, which strained relations with its key ally Washington.
Before his still unexpained death, the journalist was a columnist for the Post newspaper, where he frequently criticised the Saudi government.
Prince Khalid returns to Riyadh as a deputy defence minister.
"Part of empowering females in the kingdom is appointing the most efficient person for the position, whether man or woman", Samar al-Mogren, a Saudi writer told The Media Line.
Mrs May joined King Salman for the EU-League of Arab States Summit in Sharm El-Sheikh where she planned to urge him to use his influence to encourage Yemeni parties towards peace amid the Kingdom's strained relationship with the West. Crown Prince Mohammed bin Salman was absent from the summit.
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Bint Bandar, who was born in 1975, holds a BA degree in Museum Studies with an academic focus on the preservation of historical monuments, from George Washington University in Washington, D.C. Recently, the World Economic Forum appointed her to its Young Global Leaders program.
Saudi Arabia replaced its ambassador to Washington, a royal decree announced on Saturday, as the fallout over journalist Jamal Khashoggi's murder, the conflict in Yemen and women's rights tests relations between the two allies.
She is the 11th Saudi Ambassador to Washington.
Prince Khalid bin Salman will now be deputy minister of defense. She will now be key to that alliance as previous ambassadors have been. She had promoted greater inclusion for Saudi women in sports and breast cancer awareness, according to her official biography.
Earlier this month, a panel of British MPs and lawyers investigating the detention of women's rights activists in Saudi Arabia has concluded that their treatment may constitute torture under Saudi and worldwide law. She has long experience in the U.S., having grown up there.
"I actually do have a family that will allow me to be mobile and dynamic, but that is not the reality of a lot of women".
A high-profile businesswoman, she has worked in the public and private sector, notably as the CEO of a retail company with Harvey Nichols in its portfolio.