After graduation from the Naval War College (Japan) in 1919, he was promoted to lieutenant commander and assigned as Chief Gunnery Officer on the Iwami. Around this time, Takahashi became involved in the militant movement within the Japanese military, and helped influence the implementation of the proposal to devolve overall naval command from the Minister of the Navy to the Chief of Naval General Staff (the implementation of which was ratified by Emperor Hirohito on 25 September 1933).
From August 1923 to August 1925, Takahashi was assigned as naval attaché to the United Kingdom, during which time he was promoted to commander. After his return, he served for a year as executive officer on the Tama and became captain of the Tenryū in 1929. He was also part of the Japanese delegation to the London Naval Treaty negotiations in late 1929.
He was promoted to rear admiral on 15 November 1935, and became chief of the Second Section of the Imperial Japanese Navy General Staff. While on the General Staff, he was a strong proponent of the Nanshin-ron, urging that New Guinea, Borneo and the Celebes in the Netherlands East Indies be considered as part of Japan's stratgic sphere-of-interest. On 15 November 1939, Takahashi became vice admiral, and was given command of the Mako Guard District.
Shortly after the attack on Pearl Harbor, Takahashi served as commander-in-chief of the IJN 3rd Fleet, which included the 5th and 7th Cruiser Squadrons and the 2nd and 4th Destroyer Flotillas and formed part of the Southern Force under the command of Vice Admiral Nobutake Kondo based in Taiwan in 1941.
In January and February 1942, this force was split into the Eastern and Central Forces; the first for the invasions of Menado, Kendari and Makassar in Celebes and amphibious operations in the Banda Sea, and the second for the invasion of Dutch Borneo. Takahashi was Commander of Eastern and Central Forces during the invasion of Java. His forces included the "Direct Support Force" under Rear Admiral Shoji Nishimura, the "Second Escort Force" under Rear Admiral Raizo Tanaka, the 1st and 2nd "Naval Base Forces", under Rear Admiral Takeo Kurita, the "Third Escort Force", under Rear-Admiral Chuichi Hara, and the "First Air Group" made up of the light carrier Ryūjō and 56 transports.
On 10 March 1942, he was transferred to the newly created 2nd Southern Expeditionary Fleet, and to the newly created Southwest Area Fleet a month later. In November 1942, he was transferred back to Japan to become Commander in Chief of the Kure Naval District. He held this post until retiring from active duty in 1944.