She will star alongside Josh O’Connor, who plays a young Prince Charles in the royal drama.
“I’m absolutely over the moon, and completely terrified, to be joining so many hugely talented people on The Crown,” Fennell said. “I absolutely love Camilla, and am very grateful that my teenage years have well prepared me for playing a chain-smoking serial snogger with a pudding bowl haircut.”
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Fennell previously starred as Nurse Patsy Mount in Call the Midwife, with other acting credits including The Danish Girl, Anna Karenina, and Victoria (as Ada Lovelace).
She has also recently taken over from Phoebe Waller-Bridge as screenwriter for Killing Eve season two.
Prince Charles, played in season three by The Durrells actor O’Connor, had first met Camilla (born “Camilla Rosemary Shand”) in 1971 when they were introduced by a mutual friend.
But in 1973, Charles left for overseas service with the Royal Navy – and in his absence Camilla married Andrew Parker Bowles.
Leaked on-set photos indicate that The Crown will recreate a famous moment when Charles and Camilla re-connected at a polo match in 1975.
Charles went on to marry Lady Diana Spencer in 1981 but they divorced in 1996 and she was killed in a car crash the following year. Charles and Camilla tied the knot in 2005.
The new season of The Crown will see Olivia Colman taking over the throne from Claire Foy as Queen Elizabeth, with Tobias Menzies as Prince Philip and Helena Bonham Carter playing Princess Margaret.