Upon her arrival on 7 November she operated as a screen ship for escort carriers in Hawaiian waters and conducted experimental sonar tests with submarines before returning to Naval Station San Diego on 23 April 1946.

Arriving Yokosuka, Japan on 19 August she served as a screening ship for fast carrier forces whose aircraft flew ground support and other missions in Korea.

She took part in the siege of Wonsan harbor, supporting Korean troops with accurate and continuous gunfire, and conducted anti-submarine operations off Okinawa.

Highlights of this phase of her service include protection of the Quemoy Islands from Communist aggression in September 1954, relief of Ceylonese flood victims in January 1958, and important fleet and individual exercises during her periods at sea.

Commencing 11 August 1964, Henderson began annual cruises in Vietnamese waters, supporting the 7th Fleet amphibious and shore bombardment operations, and guarding aircraft carriers on "Yankee Station".

In December she steamed to the Gulf of Siam, where she conducted shore bombardment missions against Viet Cong positions on the Ca Mau Peninsula.

As escort for Bon Homme Richard (CVA-31), the veteran destroyer departed Hong Kong on 26 December and arrived Long Beach on 13 January 1966.

Henderson spent the next year serving as an anti-submarine warfare (ASW) school ship out of San Diego and taking part in squadron exercises out of Long Beach.

Late in July she joined in a massive, but unsuccessful air-sea search for the Hawaii-bound aircraft carrying Brigadier General Joseph Warren Stilwell, Jr., USA.

After a short restricted availability in early 1968, Henderson returned to Vietnam in April and resumed her familiar gunline and escort duties in the South China Sea.

During this tour of Asian waters Henderson also served with Bon Homme Richard (CVA-31) off the coast of North Korea in support of the captured Pueblo (AGER-2) as part of Operation Formation Star.

After a brief yard period the destroyer then spent several weeks on patrol off the Korean peninsula, as tensions remained high following the shoot down of a U.S. reconnaissance aircraft the previous year.

Returning to Long Beach on 8 May, Henderson underwent several months of inspections and certifications, which ultimately kept the warship in service in contrast to the mass 1970s decommissioning of many of her war-built sister ships.

She spent the next few weeks conducting naval gunfire support missions, including one gunnery duel with an enemy battery on Christmas Eve that earned her the Combat Action Ribbon.

After port visits to Singapore, Thailand and Hong Kong during truce talks, Henderson steamed into the Gulf of Tonkin for "Operation End Sweep" in April 1973.

The destroyer spent the majority of her time sailing in local operating areas, though the warship also conducted reserve unit training cruises to Pearl Harbor or the Pacific Northwest on an annual basis.

Highlights of this period included visits to the Portland Rose Festival (where the ship was "streaked" on one occasion by two "lassies" on a nearby cabin cruiser), being struck by a practice torpedo fired by Salmon (SS-573), and a series of excellent inspections that extended the service life of the destroyer through the end of the decade.