During the American Civil War, he commanded naval forces against Confederate forts defended by his brother Thomas F. Drayton in the Battle of Port Royal.

He served as Fleet Captain in the West Gulf Blockading Squadron and commanded the sloop-of-war USS Hartford during the Battle of Mobile Bay under Rear Admiral David Farragut.

[3] During his time in the Brazil Squadron, stationed out of Rio de Janeiro, he served as a midshipman aboard the frigate Hudson.

Promoted to commander in September 1855, Drayton served as a staff officer during the Paraguay Expedition aboard the frigate Sabine.

[5] His older brother Thomas F. Drayton, a graduate of West Point and classmate of Jefferson Davis, had resigned with the secession of South Carolina.

The Union forces captured Hilton Head, Beaufort and Parris Island and used them as a base to continue operations against Savannah, Georgia and Charleston, South Carolina.

[1] Drayton became commanding officer of the sloop-of-war Pawnee and was active in inshore operations in the waters of South Carolina, Georgia and northern Florida through the summer of 1862.

In December 1863 he began a year as Fleet Captain to the commander of the West Gulf Blockading Squadron, Rear Admiral David Glasgow Farragut.