The aerodrome was established in 1929 by Alpar, a private airline that operated within Switzerland until the outbreak of World War II. After the war, Alpar remained in business as the aerodrome's operator, supported by subsidies from the cantonal and city governments. A planned expansion in 1947 did not pass in a popular referendum, and it was not until 1950 that the first concrete airstrip was built. In 2014, Alpar was renamed to Flughafen Bern AG.

Multiple attempts to build an international airport in or around Bern instead of the small regional aerodrome at Belpmoos failed. In 1945, the national parliament decided to build the first international airport, now Zurich Airport, at Kloten near Zürich instead of in Utzensdorf near Bern, though development plans there were retained as an inter-urban airport which would require less space and thus placate local opposition by farming interests. A 1963 airport project near Herrenschwanden was abandoned because of strong popular opposition, notably by farmers, as was a 1966 project in Rosshäusern and a 1970 project in Kallnach.

In December 2016, bmi regional ceased its flights from Munich Airport to Bern after two years which it served in direct competition with SkyWork Airlines. In May 2018, RUAG announced that it would close its operation at the aerodrome in September 2018, citing declining business.

In August 2018, the aerodrome's largest carrier SkyWork Airlines declared bankruptcy and ceased all operations leaving Helvetic Airways as the sole Swiss airline serving the aerodrome with 84 percent less traffic. Since then, however, Chair Airlines, also a Swiss Airline, has begun offering services to the airport.