Career spy Blaise Metreweli to become first woman to head MI6
She will take over from Sir Richard Moore as the 18th Chief, also known as "C", when he steps down in the autumn.
"The historic appointment of Blaise Metreweli comes at a time when the work of our intelligence services has never been more vital," Sir Keir Starmer said in a statement released on Sunday night.
"The United Kingdom is facing threats on an unprecedented scale - be it aggressors who send their spy ships to our waters or hackers whose sophisticated cyber plots seek to disrupt our public services."
Of the other main spy agencies, GCHQ is also under female command for the first time.
Anne Keast-Butler took on the role in 2023, while MI5 has previously twice been led by a woman.
Until now, a female spy chief had only headed MI6 - also known as the Secret Intelligence Service (SIS) - in the James Bond movies.
Dame Judi Dench held the fictional role - called "M" in the films instead of "C" - between 1995 and 2015.
Ms Metreweli currently serves as "Q", one of four director generals inside MI6.
The position - also made famous by the James Bond films, with the fictional "Q" producing an array of spy gadgets - means she is responsible for technology and innovation.
Ms Metreweli, a Cambridge graduate, joined MI6 in 1999.
Unlike the outgoing chief, who spent some of his service as a regular diplomat in the foreign office, including as ambassador to Turkey, she has spent her entire career as an intelligence officer.
Much of that time was dedicated to operational roles in the Middle East and Europe.
Ms Metreweli, who is highly regarded by colleagues, also worked as a director at MI5.
In a statement, she said she was "proud and honoured to be asked to lead my service".
"MI6 plays a vital role - with MI5 and GCHQ - in keeping the British people safe and promoting UK interests overseas," she said.
"I look forward to continuing that work alongside the brave officers and agents of MI6 and our many international partners."
Sir Richard said: "Blaise is a highly accomplished intelligence officer and leader, and one of our foremost thinkers on technology. I am excited to welcome her as the first female head of MI6."
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