Slater entered Civil Service in 2001 joining the Cabinet Office, having previously worked for the London Borough of Islington.

[3][4][1] In July 2011, Slater moved to the Ministry of Defence as its Director-General, Transformation and Corporate Strategy, encouraged by his former Permanent Secretary Ursula Brennan.

[6][1] In October 2015, Slater was appointed head of the Economic and Domestic Secretariat at the Cabinet Office, replacing Melanie Dawes.

[6][7] In August 2020, the prime minister concluded that there was "a need for fresh official leadership” and Slater announced he was stepping down with effect from 1 September.

[8] The general secretary of the FDA union, Dave Penman, attacked the sacking in the following terms": "If it wasn't clear before, then it certainly is now - this administration will throw civil service leaders under a bus without a moment's hesitation to shield ministers from any kind of accountability."