The first unit of the KD4 sub-class, I-61 was built by Mitsubishi at Kobe, Japan. Her keel was laid on 15 November 1926 and she was launched on 12 November 1927. She was completed on 6 April 1929.
Upon completion, I-61 was assigned to the Sasebo Naval District.[2] On 24 April 1929, she and her sister ship, the submarine, combined to form Submarine Division 29,[2] [3] [4] [5] in which I-61 spent her entire career.[2] The division was attached to the Sasebo Naval District.[2]
Submarine Division 29 was reassigned to Submarine Squadron 1 in the 1st Fleet in the Combined Fleet on 1 December 1930.[2] I-61 apparently was decommissioned and placed in reserve on 11 January 1932,[5] and was transferred to the Sasebo Defense Division in the Sasebo Naval District on 10 November 1932,[2] and then to Submarine Squadron 2 in the 2nd Fleet in the Combined Fleet on 15 November 1933.[2] She was recommissioned on 1 June 1934.[2] On 27 September 1934, she departed Ryojun, Manchukuo, in company with I-62 and the submarines I-56, I-57, I-58,, I-65, I-66, and for a training cruise off Qingdao, China.[2] [3] [6] [7] [8] [9] [10] [11] [12] The nine submarines completed the cruise with their arrival at Sasebo on 5 October 1934.[2] [3] [6] [7] [8] [9] [10] [11] [12]
On 7 February 1935, departed Sasebo in company with the other eight submarines of Submarine Squadron 2 — I-53, I-54, I-55, I-59,,, and I-64 — for a training cruise in the Kuril Islands.[2] [3] [9] [13] [14] [15] [16] [17] [18] The cruise concluded with their arrival at Sukumo Bay on 25 February 1935.[2] [3] [9] [13] [14] [15] [16] [17] [18] The nine submarines departed Sasebo on 29 March 1935 to train in Chinese waters, returning to Sasebo on .[2] [3] [9] [13] [14] [15] [16] [17] [18] On 15 November 1935, Submarine Division 29 was reassigned to the Sasebo Defense Squadron in the Sasebo Naval District.[2]
On 1 December 1936, I-61 again was assigned to Submarine Squadron 2 in the 2nd Fleet,[2] and on 15 December 1938 she was reassigned to the Submarine School at Kure.[2] On 11 March 1939, I-61 suffered damage in a collision with the Japanese destroyer Yakaze off Mitajiri, Japan.[2] [4] Her Submarine School service ended when she was decommissioned and transferred to the Third Reserve in the Sasebo Naval District;[2] sources claim that this took place both on 15 November 1939[2] and on 20 March 1940.[2] [5]
On either 15 April 1940 or 15 November 1940,[2] I-61 was recommissioned, and on 15 November 1940 she was reassigned to Submarine Squadron 5 in the Combined Fleet.[2] On 8 January 1941, she collided with the gunboat Kōshū Maru south of Cape Ashizuki, Japan.[2] [4]
On 2 October 1941, with the commander of Submarine Division 29 on board, I-61 departed Sasebo with the submarine tender Rio de Janeiro Maru bound for a fleet gathering point at Murokusumi in Yamaguchi Prefecture. In the Koshiki Channel that evening, the Japanese gunboat mistook a red light she saw I-61 displaying aft of Rio de Janeiro Maru for that of a smaller vessel and misjudged her passing distance behind I-61. She collided with I-61 around 23:21. I-61 sank quickly, with the loss of all 71 men on board.[1] [4] [19]
On 20 January 1942 or in February 1942,[2] I-61′s wreck was refloated, and it was sold for scrapping in 1942. I-61 was struck from the naval register on 1 April 1942.