Aeroput became the flag carrier of the Kingdom of Yugoslavia and, by the opening of numerous airfields throughout the country, significantly improved connections between the various regions.

Besides providing passenger, mail, and cargo service to its domestic destinations, Aeroput inaugurated its first regular scheduled international route, Belgrade–Zagreb–Graz–Vienna, in 1929.

During the 1930s, it expanded by opening new routes to other destinations in Austria, Czechoslovakia, Hungary, Romania, Bulgaria, Greece, Turkey, Albania, and Italy.

According to IATA in 1988, JAT was the tenth largest airline in Europe by flying to 76 destinations in 39 countries, which included long-haul flights to Los Angeles, Chicago, Detroit, Cleveland, New York, Montreal, and Toronto in the west, and Beijing, Calcutta, Kuala Lumpur, Singapore, Melbourne and Sydney in the east.

An aging fleet and lack of investment made the airline unprofitable, so the Serbian government sought a strategic partner for the company.

On 23 June 2016, Air Serbia's non-stop flights between Belgrade and New York commenced using an Airbus A330-200 leased from Etihad partner, Jet Airways.

The goal was to focus on net profit, a new fare structure, new sales channels, and offer additional services that would increase efficiency.

This service replaced its previous inflight catering and offers one of two menus based on flight length and type of aircraft operating the route.

In April 2022, it was reported that a NATO military aircraft had trailed an Air Serbia flight as it left Russian airspace.

The plane was welcomed by a water salute ceremony, marking the first direct flight between Shanghai and Belgrade, the capital city of Serbia.

[41] The majority of Aviolet charter flights were operated during the peak holiday season, which runs from June to September.

Located near Nikola Tesla Airport, the company prepares and handles inflight meals for Air Serbia, as well as other carriers flying to and from Belgrade.

Featuring Serbia's national colours – red, blue, and white – the design, with its graphical elements and details, is based on Serbian medieval art.

In 2013, the airline launched the "Living Legends" initiative, which pays tribute to famous Serbian citizens who have made positive contributions to society, both in Serbia and abroad.