[7] The Mi-38's development was carried out by Kazan Helicopters since early 1980s[2] and a mockup was first shown during the 1989 Paris Air Show.

After the dissolution of the Soviet Union in 1991, Kazan Helicopters went into collaboration with Eurocopter that was to adapt the Mi-38 for international market.

[12] On 30 December 2015, Rosaviatsiya certified the Mi-38, completing the testing and certification program and allowing for the delivery of the first production model.

[15][16] The new variant was developed to meet the Russian MoD's new requirements for the helicopter and due to international sanctions imposed on Russia, all of its components, including engines and avionics, are Russian-made.

[11] Deputy Managing Director at Kazan Helicopters Vadim Ligai stated that the Mi-38 can now carry up to 40 passengers.

[19][20] In 2023, the Government of Zimbabwe was gifted an Mi-38 helicopter by Russian President Vladimir Putin, during the Second Russia-Africa Summit hosted in Saint Petersburg.

[21][22][23] This follows the delivery of a number of Kazan Ansat helicopters for the Zimbabwe Republic Police, as well as a new air ambulance service for the country.

[24][25] In March 2024, Kolyma Aviation received two Mi-38 helicopters for operating commercial flights connecting Magadan Oblast.