Standley then reported to the armored cruiser USS Pennsylvania on 3 November 1910 and was navigator of that ship until becoming aide to the Commandant of the Mare Island Navy Yard at Vallejo, California.

Returning to the Naval Academy on 14 October 1916, as Assistant to the Superintendent in charge of Building and Grounds, Standley later served for 11 months as Commandant of Midshipmen.

Under his direction, the new seamanship and navigation buildings were constructed and over $4,000,000 spent in enlarging Bancroft Hall to accommodate the increased number of midshipmen appointed during the World War I period.

Breaking his flag in his former command, California, the admiral remained at sea until 1 July 1933, when President Franklin Roosevelt appointed him Chief of Naval Operations, replacing William V. Pratt.

Unlike Pratt, who had been content being primus inter pares among the bureau chiefs of the Navy, Standley asserted his position over them and treated them as his subordinates.

The argument grew severe enough for Standley to bring it directly to the President who decided to uphold the status quo and the CNO's limited authority.

In addition, during his tenure as CNO, Standley initiated the Vinson–Trammell Naval Bill that provided for establishing, building, and maintaining the navy at treaty strength.

Recalled to active duty on 13 February 1941, Standley served as naval representative on the planning board of the Office of Production Management (OPM) for seven months.

After leaving the OPM in the autumn of 1941, Standley served as the American naval member on the Beaverbrook-Harriman Special War Supply Mission to the Soviet Union.