In the hugely significant intervention, she expressed her "sincere wish" that Camilla will be known as Queen Consort when the Prince of Wales becomes King.
As she reached her 70th year on the throne, Elizabeth II, in the twilight years of her reign, set out her hopes for her daughter-in-law, once a royal mistress and now certain to be called Queen and crowned at Charles's side.
Elizabeth II, using the rarest of Jubilees to put her affairs in order on a public platform, also shared her succession support for her eldest son as monarch.
The Queen, 95, said in the written message: "I would like to express my thanks to you all for your support. I remain eternally grateful for, and humbled by, the loyalty and affection that you continue to give me.
"And when, in the fullness of time, my son Charles becomes King, I know you will give him and his wife Camilla the same support that you have given me; and it is my sincere wish that, when that time comes, Camilla will be known as Queen Consort as she continues her own loyal service."
The Queen who acceded to the throne on February 6 1952 on the death of her father George VI, also renewed her lifelong pledge of duty, despite approaching her 96th birthday this year.
She also paid tribute to the late Duke of Edinburgh for the sacrifices he made as consort, thanked her family for their support, and made reference to the Queen Mother's role as a Queen Consort.
Camilla will take the role of consort when Charles becomes king.
The Queen wrote: "I am fortunate to have had the steadfast and loving support of my family. I was blessed that in Prince Philip I had a partner willing to carry out the role of consort and unselfishly make the sacrifices that go with it.
"It is a role I saw my own mother perform during my father's reign."
Camilla would technically have been Queen when Charles acceded to the throne, and only legislation would have prevented it.
Royal aides had previously insisted Camilla did not want to be queen and that she "intended" to be known instead as Princess Consort - the first in British history - instead.
The careful use of the verb "to intend" left this open to change in the future.
Any mention of "Princess Consort" was removed from Charles's website during a revamp in 2018.
Former BBC royal correspondent Peter Hunt said: "This is the most extraordinary message. The Queen is ensuring the transition, when it comes, to her son as king is as seamless and trouble free as possible.
"She's future-proofing an institution she's served for seventy years. And for Camilla, the journey from being the third person in a marriage to queen-in-waiting, is complete."
Prime Minister Scott Morrison has paid tribute to Queen Elizabeth upon her reaching her 70th year as monarch.
"Understandably, The Queen traditionally does not mark this day with any joy, as the day marks the anniversary of the passing of her father," Mr Morrison said in a statement on Sunday.
"Still, today marks an extraordinary milestone.
"For over half of our history as a federation, The Queen has been our monarch. Most Australians have known no other sovereign. She has been a constant presence in a changing world."
Mr Morrison said appropriate Australian celebrations to mark the platinum jubilee would be staged later this year.
AAP with The Project