Slessor commanded No. 4 (Army Cooperation) Squadron, which flew Bristol Fighters out of RAF Farnborough, from April 1925 to October 1928, when he joined the air planning staff at the Directorate of Operations and Intelligence at the Air Ministry. He attended the Staff College, Camberley, in 1931, and was appointed RAF Directing Staff Officer there in January 1932. Slessor was promoted acting wing commander on 1 January 1932 (substantive on 1 July). He became Officer Commanding No. 3 (Indian) Wing at Quetta in March 1935, and was awarded the Distinguished Service Order for operations in Waziristan between 25 November 1936 and 16 January 1937.