1937 saw construction of the first concrete runway; it measured 405 by 21 metres (1,329 by 69 ft). In 1938 eight airlines were flying to Geneva: Swissair, KLM, Lufthansa, Air France, Malert (Hungary), AB Aerotransport (Sweden), Alpar (Switzerland) and Imperial Airways (UK).

During World War II, the Swiss authorities forbade all flights from Switzerland, but expansion of the airport led to increasing its area to 95 hectares (230 acres) and extending the main runway first to 1,000 by 50 metres (3,280 by 160 ft). A further 200 metres (660 ft) of runway was added near the end of the war as well as provision for future expansion to a length of 2,500 metres (8,200 ft).

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The airport has a single concrete runway (04/22), which is the longest in Switzerland with a length of 3,900 m (12,795 ft) and one of the longest in Europe, making it open to use by aircraft of all existing sizes. Adjacent to the commercial runway is a smaller, parallel, grass runway for light aircraft. Since its opening, the runway had been known as 05/23 until September 13, 2018, when it was changed to 04/22 due to the North Magnetic Pole moving. Usually, runway 22 is used when the wind is calm. If the wind is stronger than 4 knots and in a direction going from 320 to 140 degrees, then runway 04 will be used.