While patrolling submerged 5 nautical miles (9.3 km; 5.8 mi) north of Pointe des Almadies, Blackfish sighted a Vichy French convoy of three cargo ships escorted by a destroyer.

She eventually headed north, and on 26 November 1942 she rendezvoused with the Royal Navy Hunt-class destroyer HMS Lauderdale off The Lizard on the southwest coast of England and then steered toward Scotland.

She returned to Rosneath, mooring there on 18 January 1943, thus ending her second war patrol with little to show for it other an account of a minor episode of laryngitis among her crew, a few photographs, and some intelligence on merchant ships and fishing vessels.

On several occasions, she received notification of the passage of the Vichy French ships Winnetou, Livadia, and Nordfels steaming from Bilbao to Bordeaux, France.

At last, at 17:49, Blackfish clearly observed German colors and identified both ships as converted trawler-type submarine tender vessels with guns mounted fore and aft.

Gale-force winds, rain, and poor visibility hindered all training efforts, and by 15:00 Blackfish had shaped a new course, proceeding in company with the former French Navy minesweeper HMS La Capricieuse to Muckle Flugga in the Shetland Islands.

In his reflections on the patrol Lieutenant Commander Davidson observed that "the excessive smoking and steaming of the main engines in cold weather is a very serious military hazard and an immediate remedy is considered vital."

Upon her arrival at Groton, Blackfish underwent repairs, during which she replenished her supplies and her crew conducted training for their upcoming deployment to the Pacific for the war with Japan.

En route to her patrol area, she conducted multiple night radar training exercises on 20 October with her escort, the submarine rescue vessel USS Coucal (ASR-8).

While assigned to a scouting line on 3 November 1943, Blackfish was on the surface when she encountered a Japanese convoy of two merchant ships, which her crew estimated at approximately 4,000 to 6,500 gross register tons, escorted by one patrol boat.

Twenty minutes passed before she suddenly heard several explosions, which her crew believed to be depth charges, and the Japanese convoy changed course and disappeared.

Davidson observed that Blackfish′s rudder was exceedingly loud, and he believed that the Japanese ability to locate Blackfish was directly related to her inability to keep quiet.

Although Blackfish had attempted both of her primary attacks on Japanese convoys at excessive range, her commanding officer and crew "benefited greatly from the experience and will undoubtedly inflict greater damage to the enemy on the next patrol," according to a post-patrol assessment of her performance.

Esorted by Coucal and in company with the submarine USS Redfin (SS-272), Blackfish set out from Milne Bay on her seventh war patrol on the morning of 25 December 1943.

As the opportunity faded, Davidson remarked "our last hope was one of the patrolling destroyers, which we managed to close to 3,000 yards (2,700 m) but without a very good set[-]up because of the constant changes of course and speed.” Given the circumstances, Blackfish pulled back.

During the early morning hours of 8 January, one of the destroyers in the convoy came within sight again and Blackfish turned toward her on the surface and put all four of her diesel engines "on the line" to get into an attack position.

While in her patrol zone in the early morning of 3 February 1944, Blackfish sighted smoke and subsequently discovered a Japanese convoy consisting of two medium-sized merchant ships, two Fubuki-class destroyers, and one other unidentified escort of approximately 1,000 displacement tons.

After taking on provisions at Pearl Harbor, Blackfish departed on 21 May 1944 and arrived at Bethlehem Steel Corporation’s Submarine Repair Base at San Francisco, California, on 27 May.

Blackfish began the patrol on 23 September 1944, departing Pearl Harbor and heading for Saipan in the Mariana Islands in company with Seadragon and Shark.

Both disgusted and mystified by the misses, Sellars decided it prudent to refrain from "wasting" more torpedoes on the destroyer and Blackfish returned to her patrol area empty handed.

The daily sickening of the crew upon surfacing persisted, and no cause for the condition could be determined; some crewmen speculated that it was from the air, a test of which indicated the presence of only one percent carbon dioxide, well within safety limits.

In addition to the sickened crew, an inordinate amount of radio traffic coming across the frequency — a result of Task Groups 17.11, 17.14, and 17.15 operating in the same area — impaired Blackfish′s communications.

By 25 October 1944, a majority of Blackfish′s crew had regained their health, with only a few lingering cases, and Shark and Seadragon reported that they were out of torpedoes due to the numerous attacks they had executed in the preceding weeks.

On 4 February, she received word that the sampan she attacked might have been Chinese, to which Sellars responded that he "considered that possibility each time before shooting but with return fire, attempts to ram, regular patrol in pairs, and non-junk-like hulls, the enemy indications overruled."

While patrolling in her lifeguard area, Blackfish came across several naval mines and attempted to detonate them with .45-caliber (11.43 mm) Thompson submachine gun fire, which proved ineffective.

On 3 August 1945, a major storm front moved in and broke with full fury, prompting Blackfish to dive to 150 feet (46 m), Sellars noting that he doubted "if we could ride this one out on the surface."

A few days after the storm, what Sellars described as "swarms of American planes" headed toward Kogoshima Kaiwan, and Blackfish was called upon to rescue several downed aviators.

Several more cramped days at sea passed, but at last Blackfish arrived at Guam on 14 August 1945 and moored to the starboard side of the submarine tender USS Fulton (AS-11), ending the patrol.

Although she made no attacks on Japanese shipping, she had rescued six U.S. Army Air Forces personnel, and her crew was authorized to wear the Submarine Combat Patrol Insignia.

After transiting the Panama Canal and making brief stops at New York City and Camden, New Jersey, she arrived at Naval Submarine Base New London in Groton, Connecticut, in September 1945.