In a stinging attack on the First Minister and her Nationalist colleagues, the Scottish Conservative leader said they were "cranking up the grievance machine in an attempt to push people towards the exit door" and the break-up of Britain.
In a keynote speech to the London School of Economics on Monday evening, Ms Davidson argued that Britain must reject “economic nationalism” in the Brexit process but instead seek to maintain itself as an outward-looking, free-trading country.
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She warned that people must "not dismiss the challenge the SNP poses, no matter how weak the case for independence may seem".
Despite Scotland having voted against independence in 2014, the party leader said that last year’s European Union referendum - when most Scots voted to remain part of the EU but the UK voted to leave - meant there was now the "grim possibility" of another ballot on Scotland’s future.
However, she said that while some people might think that “separation is inevitable" in the "seemingly endless" constitutional turmoil, she claimed the Brexit vote had weakened the case for Scotland leaving the UK.
"Despite the uncertainty, the insecurity, and the challenges, the case for the Union - our Union - remains strong, if not stronger, than it ever has,” Ms Davidson declared.
"We just have to ensure that we make the right case, for an outward-looking Britain that provides us all with the opportunities and the stability we all crave."
In the wake of the vote to quit the EU in 2016, the SNP was, the Scottish Tory leader claimed, "itching to get its own campaign bus into gear", warning that the Nationalists would have "learnt from the tactics" of the successful Leave campaign.
"The case for the Union must be made afresh and we have to persuade people once again that our own Union of nations still works for us all," the Tory MSP insisted.
Ms Davidson noted how this would throw up something of a Brexit paradox.
"Because while Brexit has provided the means for Nicola Sturgeon to crank up her independence campaign once more, it has also made that case weaker and more illogical than ever."
Scottish Government figures show exports from Scotland to the UK were worth £49.8 billion in 2015; this is four times the value of exports to the rest of the EU, which amounted to £12.3nm.
"If everyone in Scotland agrees that free trade with Europe is important - and we do - it is literally impossible to deny that trade with the rest of the UK matters four times as much," the party leader argued.
Yet she claimed the SNP "has no intention of using economics to make the case for independence" if there were a fresh referendum. "Instead,” Ms Davidson said, “it is already cranking up the grievance machine in an attempt to push people towards the exit door."
The leading Tory, who played a prominent part in the campaign to keep Britain in Europe, said that while her preference was for the UK to stay in the EU, there was no reason why it could not make a success of things outside the Brussels bloc.
"As a country that expounds the virtues of free trade and solidarity with our allies and neighbours, knowing that this is the way to ease poverty, to build a more just world, and to make us here at home safer and more secure.”
She added: “I lost the case for one Union last year. I have absolutely no intention of losing another. But if we are to win the argument, we must step up and demonstrate that our own Union is a living, breathing being which can change when required, which is responsive to people's needs and which is open to the world around us."
In response, an SNP spokesman branded Ms Davidson the “Brexiteers' apologist-in-chief”, who had shamelessly sold out on her commitment to keep Scotland in the European single market.
"Ruth Davidson is resorting to fantasy and delusion in trying to deny the economic catastrophe a Tory hard Brexit threatens Scotland with.
"We face being dragged out of the world's biggest single market - which is around eight times larger than the UK's alone - against our will, which shows that Theresa May and the Westminster Tories now think they can do anything they want to Scotland and get away with it,” he added.