Ms Khan was the first agent to be infiltrated into enemy occupied France to aid the French Resistance during the Second World War, landing in the country in June 1943.
Working with the Paris Resistance group, she aided the allies by relaying messages back to Britain.
She was eventually caught and taken to the Gestapo’s headquarters, where she refused to cooperate with the Nazis and decode seized messages.
Ms Khan was then taken to the Dachau concentration camp, where she was executed on September 12 1944.
She was posthumously awarded the George Cross in 1949.
On Tuesday, Camilla attended the RAF Club to unveil the portrait and to announce that the room it will hang in will be renamed the Noor Inayat Khan Room.
Speaking to attendees, she said: “I feel very humble to unveil such a brave woman.
“I am delighted to name this room after her.
“It’s a wonderful painting.
“It’s very difficult, as I said, to do posthumously.”
The portrait was painted by artist Paul Brason.
Speaking to the PA news agency, he agreed that it was a difficult portrait to paint.
“One of the difficulties about painting a portrait of someone who was operating undercover, particularly in the Second World War, is that people who work undercover don’t like photographs being taken of them.
“So that means, in regards to the reference material, there is not very much of it.
“Certainly none of it in what, dare one calls it, her professional capacity, because she would avoid it.”
However, he said he was able paint the portrait by working from a handful of photographs of Ms Khan.
Ms Khan’s cousin, Mahmoud Khan, 95, said it was a “excellent” likeness.
“It is an excellent likeness,” he said.
“That is what struck me most, that the painter did so much to bring her personality to life.
“It is truly splendid.”
The Queen also met with members of staff at the RAF Club, posing for a photo with them before she left.