Campaign groups Uplift and Greenpeace have brought judicial reviews at the Court of Session in Edinburgh, arguing that the government illegally granted operators permission to exploit the fields.
Lawyer Ruth Crawford, representing Greenpeace, said it was "agreed by all that decisions made on Jackdaw and Rosebank were unlawful because Scope 3/downstream greenhouse gas emissions were not assessed in environmental statements submitted by interested parties".
Scope 3 emissions are essentially all carbon emissions indirectly generated by a business.
Crawford urged judge Andrew Stewart to ignore arguments from energy firms behind the schemes about the cost of pausing development.
Shell, which owns the Jackdaw gas condensate field 155 miles (250 kilometres) east of the Scottish city of Aberdeen, has said stopping work was "a highly complex process, with significant technical and operational issues now that infrastructure is in place and drilling has started".
Production had been due to start next year, with Shell saying it would provide enough fuel to heat 1.4 million UK homes.
Equinor, the majority owner of Rosebank oil field, 145 kilometres off the Shetland Islands in Scotland's far north, has said the development would create jobs and be vital for UK energy security.
Rosebank is the UK's largest untapped oil field, estimated to contain up to 300 million barrels. Drilling had been due to begin between 2026 and 2030.
- 'Narrow window' -
Before the case, which is due to last four days, hundreds turned out to demonstrate outside the court, in a celebratory mood given recent rulings that the UK government had granted permissions unlawfully by failing to take into account all emissions from burning oil and gas.
A ruling in favour of the campaigners would mean that operators would have to resubmit environmental assessments for approval before drilling can start.
Former Scottish National Party lawmaker Tommy Sheppard called the case "the granddaddy because it is so big". "The case will be applied to the decision-making process in general," he told AFP.
"There were 100 licences granted by the last Conservative government in its final dying months. All of them will now be under question."
The campaigners' confidence comes from a UK Supreme Court ruling in July that the previous Conservative government should have considered the carbon emissions of burning extracted oil and gas, not just of extracting it.
The incoming Labour government then announced it would not contest the Rosebank and Jackdaw case, leaving the oil companies alone to fight the legal challenges.
"We are on the precipice of a massive victory for the climate," said Uplift campaigner Lauren MacDonald.
The group's executive director Tessa Khan said it sent a message to the energy industry and that the "window for approval has really, really narrowed".
- Renewables -
Prime Minister Keir Starmer, in Baku, Azerbaijan for the UN climate change summit, on Tuesday said the UK would aim to reduce greenhouse gas emissions by 81 percent on 1990 levels by 2035, as part of government plans to reach net-zero by 2050.
Sheppard said the increased economic costs would force energy companies to look towards developing the renewables sector, provided the government gives the necessary investment and incentives.
At the same time, governments in oil-generating countries like Scotland must tread a fine line in balancing the longer term threats of rising temperatures with the shorter term risks of job losses in the sector.
Energy historian Ewan Gibbs, from the University of Glasgow, pointed to potential parallels with the breakdown of social cohesion caused by the closure of the UK's coal mines in the 1980s without a plan for those made redundant.
Sheppard said it was important that those affected by net-zero transition plans be reskilled and retrained to enable them to benefit from new jobs being created by clean energy technologies.
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