INGHAM departed Hong Kong on 29 November 1945 and steamed for Saipan, arriving there on 5 December. She then proceeded to set course for home, stopping at Pearl Harbor and then sailing through the Panama Canal. INGHAM arrived in New York on 6 January 1946 and then steamed on to the Charlestown Navy Yard, arriving there on 7 April. She then underwent a reconversion back to her peacetime configuration, including the removal of the majority of her armament. Her superstructure was cut back to her pre-war configuration as well, all in preparation for her to undertake what would become her primary peace-time task, as well as that of her sister 327s, that of operating on ocean-weather stations. With the post-war boom in trans-Atlantic air traffic, the Coast Guard's operation of these weather stations became even more important and a number of newer stations were added further out to sea. Here cutters, serving on these stations, carried personnel from the U.S. Weather Bureau, who would make daily meteorological observations and report their findings to the U.S. Weather Bureau. They also served as a mid-ocean navigation aids, communications relay stations and as search and rescue platforms when needed. The ocean station program was permanently established by multi-national agreement soon after the end of World War II. The Coast Guard was then assigned the duty of manning those stations for which the U.S. accepted responsibility. As the 327s completed conversion to ocean station vessels, each immediately deployed to their new stations. The TANEY went to the Pacific while the other 327s remained in the Atlantic.
INGHAM completed her modifications in July 1946, and then sailed to her new homeport of Norfolk, Virginia, arriving there on 28 July 1946. She then underwent training and then departed for Boston, arriving there on 10 August and then steamed for duty on Weather Station Able by way of Argentia, arriving on station on 8 September 1946. She remained on station for three weeks before returning to Argentia on 3 October. For most of the next twenty years, INGHAM alternated duty between the various weather stations (soon to be known as simply "ocean stations") along with her sister cutters. Her other assignments included sailing on Academy cadet cruises during the summer months, undertaking oceanographic surveys, providing medical aid to ailing seamen on the high seas, towing ships out of danger, assisting other merchant vessels that were disabled, and search and rescue duties.
In April and again in June of 1949 she served on Ocean Station Easy. In August of that same year she served on Ocean Station Charlie. In January of 1950 she served on Ocean Station Easy and in March and April of 1950 she served on Ocean Station Dog. From 4 June to 1 September 1950 she served on a cadet cruise to Europe. From 4 to 24 November 1950 she served on Ocean Station Able where she again served from 10 to 25 December of that same year. From 3 to 24 February 1951 she served on Ocean Station Charlie and then from February to March of 1953 she served on Ocean Station Hotel. Later that year, from May through June of 1953 she served on Ocean Station Delta. She served on Ocean Station Bravo from November to December of 1953. During February of 1954 INGHAM served on Ocean Station Cola. From April to May of 1954 she served on Ocean Station Hotel and on Ocean Station Echo during July of 1955. From July to August of 1956 she served on Ocean Station Bravo and in December of that year she served on Ocean Station Charlie. In May of 1957 she served on Ocean Station Echo. From February to March of 1958 she served on Ocean Station Delta and again at Delta from May to June of the same year. From September to October 1959 she served on Ocean Station Bravo and from November to December of 1959 she served on Ocean Station Charlie.
INGHAM served on Ocean Station Delta from April to May of 1960 and then from June to July of the same year she served on Ocean Station Bravo. In June to July of 1961 she served on Ocean Station Delta and then on Ocean Station Charlie from 12 June to 3 July of 1964. She served on Ocean Station Delta from 24 August to 16 September of 1967 and from 24 November to 17 December of the same year she served on Ocean Station Charlie. She then served on Ocean Station Echo from 26 February to 20 March of 1968.
Her humanitarian missions were many and she contributed her services in support of scientific operations as well. On 27-28 November 1950 she medevaced a patient from the MSTS Henry Gibbons and transported him to St. John's and provided medical assistance to a crewman on board the Greek merchant vessel SS Calli in March of 1956. In April of 1961 she was called upon to assist the merchant vessel SS Cape York, which reported having a fire in a cargo hold, while that vessel was moored in St. George's Harbor, Bermuda. She conducted an oceanographic survey in June and July of 1964, becoming the first Treasury class cutter to undertake such a mission. On 1 May 1965 the Treasury class vessels were re-designated as High Endurance Cutters or WHEC. This designation indicated a multi-mission ship able to operate at sea for 30-45 days without support and INGHAM was then re classified as WHEC-35. INGHAM sustained a fire that destroyed her CIC on 10 May 1965. She helped fight a fire on board the merchant vessel SS Caldas on 27 February 1967 50 miles east off Chincoteague, Virginia. In July 1967 she medevaced an injured crewman from the merchant vessel SS Lancing 360 miles northeast of Miami after undertaking another cadet cruise.