Pete Wishart and Stewart McDonald both resigned on Thursday, exposing clear rifts among within the Westminster group just days after Mr Flynn replaced Ian Blackford as its leader.
As Mr Flynn, the MP for Aberdeen South, begins his reshuffle, the team’s overhaul is understood to be less about just putting MPs in new roles, and more a total revamp of how the group works.
Several MPs told The Scotsman for too long the party had mirrored the UK state and given jobs to keep people happy, with Mr Flynn’s revamp designed to represent top-down change.
The party is believed to be considering creating and expanding jobs, rather than just having straight like-for-like shadow roles in areas such as foreign affairs and defence.
The overhaul comes with Chancellor Jeremy Hunt set to launch in Edinburgh a major reform of the UK’s financial sector, with plans to rip up red tape and replace reams of EU regulations that will put the UK Government once again at odds with the SNP’s pro-Europe agenda.
Dubbed the “Edinburgh reforms”, the changes will be announced by the Chancellor in the Scottish city today as he heralded the “golden opportunity” Brexit provided to reshape the rules governing the financial sector.
Mr Hunt will set out a package of more than 30 regulatory reforms, with plans to “review, repeal and replace” hundreds of pages of EU regulations ranging from disclosure for financial products to prudential rules governing banks.
The overhaul of the SNP’s Commons front bench comes little more than a fortnight since the Supreme Court ruled the Scottish Parliament could not legislate for an independence referendum without the UK Government’s agreement.
A poll published this week by Ipsos Scotland showed support for Scottish independence had risen to 56 per cent, with don’t knows excluded, in the wake of the Supreme Court judgement.
SNP MP Alyn Smith said: “Change will do us no harm, and after the Supreme Court judgement we have a job to do to build the independence case in Europe.
“The group for good reason was structured on shadowing the roles at Westminster. Stephen is bringing a focus on what we need to do to deliver independence.”
It comes as Mr Wishart, the SNP’s MP for Perth and North Perthshire, announced his resignation from the party’s front bench in a scathing letter.
Quitting as the group’s DEFRA spokesman, he said: “We have never had an opportunity to discuss your plans for the group, neither when you were canvassing opinion for a leadership challenge, nor at any point during the very short campaign for the leadership itself.
"I note that you hope to bring positive change to the way the group is run and that you wish to re-set the relationship with colleagues in Government and the Scottish Parliament.
“I remain bemused as to the reasons why you felt it was necessary to seek a change in our leadership, particularly when we see yesterday’s opinion poll, which shows support for independence at a near all-time high and support for the SNP at Westminster at an unprecedented 51 per cent.
“Usually change of this significance accompanies failure, whereas we are looking only at sustained and growing success as a movement and party. I am sure that this is something that will become apparent to me during the course of your leadership.
“I also look forward to learning first-hand what you hope to do differently in the day-to-day management of the group.”
However, the Perth and Perthshire North MP said Mr Flynn had his “full support”, adding “I remain at your service if you do wish to make use of my experience in the Westminster group.”
Responding to the letter, Mr Flynn thanked Mr Wishart for his “exemplary service” on the SNP front bench. He added: “As ever, my door remains open and I look forward to working with you as we support colleagues in Holyrood, hold the Tories to account and work to deliver independence.”
Mr McDonald also resigned from his role as the party's Westminster defence spokesperson after five-and-a-half years.
Despite having backed defeated challenger Alison Thewliss for leader, Mr McDonald’s resignation is a blow to Mr Flynn, who had hoped to keep on the experienced and popular MP.
In a letter hinting at divisions within the party, he said: “Being the SNP’s defence spokesperson is one of the toughest roles in the party, but one I embraced with enthusiasm and have loved every minute of. I want to thank my friend, Ian Blackford, for the opportunity to take on the defence brief and for the active support he showed me throughout.
“The party today is in a strong position. The latest polling is stunning – even more so when you consider that we are entering our 16th year in government.
“We are at our best when we collaborate as a united party and sell a modern vision of what Scotland can still achieve – a confident case that’s rooted in understanding the challenges of today, offers credible, innovative solutions and builds a coalition of voters behind our ideas.
“I’m sure the new leadership team at Westminster will keep this at the forefront of their mind and work in that spirit across the party.”
In other front bench changes, Owen Thompson has been replaced as the party’s chief whip at Westminster by Martin Docherty-Hughes, the West Dunbartonshire MP.
The overhaul comes as Scottish Secretary Alister Jack wrote to the new Westminster leader congratulating him, and inviting him to Dover House, the Scotland office on Whitehall.
Mr Jack also stressed his hope for co-operation, saying it was “essential” Scotland’s two governments worked together.
He said: “Your predecessor enjoyed constructive and cordial relationships with ministers across the UK Government and I know you will wish to develop similar links.
“It is essential that Scotland’s two governments work together on projects that will benefit the people of Scotland. As you know, the UK and Scottish governments have collaborated successfully on our city and region growth deals and on our exciting, soon-to-be-announced, Freeports programme.
“Together we are already creating jobs and boosting the Scottish economy. But I believe there are more areas where we can work together.
“The UK and Scottish governments should be working more closely to improve transport links across the UK, helping to strengthen the internal market that so many businesses and jobs rely upon.
"The people of Scotland rightly expect their two governments to improve all our lives. I am determined we approach the serious issues facing our country in that spirit.”
Since standing down, Mr Blackford has insisted he would have won if he’d taken the leadership challenge to a vote rather than stepping aside.
He told TalkTV: “I could have seen this off, I believe I would have won if I’d put myself forward.
“Some people have a different way of wanting to do things and I think its fair to say that some people probably wanted to see the end of my backside off the front bench. That’s fine. They’re entitled to that.”