The company blames disruption caused by the COVID-19 pandemic for the flights, which it calls accidental. The penalty will be halved if it avoids any similar transgressions for one year.
Virgin Atlantic has said it accidentally broke a US-imposed ban on flying over Iraq after it was fined more than £870,000 by US authorities.
The US Department of Transportation hit the airline with a penalty of $1.05m (£870,700) after it found a "significant number" of the carrier's flights between the UK and India crossed restricted airspace in Iraq between September 2020 and September 2021.
At the time, the US Federal Aviation Administration (FAA) banned US airlines' flights at any altitude because of "heightened militia activities and increased tensions in Iraq".
The US federal agency still bars civilian planes below 32,000 feet.
Virgin Atlantic was subject to FAA restrictions at the time, the department said, because it was operating in partnership with Delta Air Lines, the US firm which owns 49% of the British-based company.
The companies have a so-called code-sharing agreement in which Delta put its own "code" on some Virgin Atlantic flights and sold seats as if they were Delta airplanes.
In a consent agreement posted on Tuesday, Virgin Atlantic said the overflights were inadvertent.
The airline said it followed FAA restrictions on code-sharing flights in the past and the violations were caused by disruptions and staff shortages brought on by the COVID
The company said it immediately rerouted flights after learning of the violations.
Half of the fine, or £435,350 ($525,000), will be waived if Virgin Atlantic avoids similar transgressions for one year, the Press Association said.