The European Court of Justice has fined France 20m euros (£14m; $24m) and imposed an extra rolling penalty for flouting EU fishing rules.
France is being penalised for endangering fish stocks
France will have to pay 57.8m euros every six months if it fails to comply.
The fines are the biggest ones the court has levied against a member state to date, the court confirmed.
The head of France's National Fisheries Committee (CNPMEM) reacted angrily to the fines, calling them "completely unacceptable pressure on France".
It is the first time the court has imposed such a "combination" fine on a member state.
Pierre-Georges Dachicourt of the CNPMEM told France Info radio that the court was unfairly singling the country out for criticism.
"Tonnes upon tonnes of small fish are unloaded in Spain, Portugal. There is fishing over and above the quotas in Scotland, Britain and elsewhere, and you never hear anything about it. People always point the finger at France," he said.
"We follow the letter of European rules," he insisted.
The court press service told the BBC News website that no fines were currently envisaged for any other EU members apart from France for fishing violations.
In earlier rulings, Spain was fined 624,105 euros annually over dirty bathing water and Greece was fined 20,000 euros daily for breaching EU rules on sewage treatment.
The court said France must above all carry out systematic inspections of nets and unloading of fish in accordance with EU rules.
It criticised France for "letting undersized fish be offered for sale and maintaining a lax attitude" towards infringements.
For nearly 15 years the court has been battling France over the mesh sizes of its fishing nets and rules on catching undersized fish.
The first ruling against France came in 1991, when the court ruled that Paris was in breach of EU fisheries laws.
Ten years later the European Commission again complained to the court that France was flouting EU law.
A daily or six-monthly fine is aimed at forcing a member state to comply with a previous order.