Critics of Defence Secretary Gavin Williamson have said his suggestion that Islamist fighters should be hunted down and killed could put British soldiers at risk of prosecution.
Liberal Democrat defence spokesman Lord (Menzies) Campbell said the Defence Secretary appeared to be endorsing breaches of humanitarian law.
Meanwhile, labour MP and former paratrooper Dan Jarvis said his comments were "morally, legally and practically wrong".
Prime Minister Theresa May's official spokesman said measures already existed to cancel IS fighters' British passports and ensure that those who return to the UK face police investigation and possible prosecution.
And the Independent Reviewer of Terrorism Legislation, Max Hill QC, took to Twitter to say:
"My only comment on the Defence Secretary's views about UK citizens fighting for IS: criminal prosecution inevitable in most cases where UK citizens return, and where evidence of committing serious criminal offences."
In an interview with the Daily Mail Gavin Williamson praises British forces and their approach to tackling the threat of terrorism:
"Our forces are right across the globe degrading and destroying that threat, making sure that these people who want to bring destruction, death, bloodshed onto our streets aren’t able to come back,"
"Every day we have got British service personnel making a difference to make sure some of those people that want to cause that harm are never able to come back to this country. That is something I am incredibly proud of".
Figures released by the MoD show that Britain has dramatically increased it's drone strikes, from just one Reaper strike in 2015 to 31 strikes in 2017.
Mr Williamson pledged that the Armed Forces stand ready to do whatever is needed to keep Britains safe from terror attacks.
Back in October, the terror laws watchdog sparked rows when they suggested authorities should look to "reintegrate" the "young" and "naive" jihadis who travel to war zones, rather than prosecute them, on their return to the country.
Max Hill QC, the Independent Reviewer of Terrorism Legislation, spoke of "losing a generation" of men and women by automatically using the courts to punish them.
However the Defence Ministers, in his interview with the Daily Mail, made some of the most severe comments made about the situation:
"Quite simply, my view is a dead terrorist can’t cause any harm to Britain".
He added that not a single British citizen who has fought for Islamic State should be allowed back into the UK and he was willing to use air strikes against the 270 UK citizens in Syrian and Iraq.
Mr Williamson also said that even those who have fled to other countries will be found and prevented from returning to the UK. It is believed they will have their passports confiscated if they try to cross over international borders.
"There is no safe space for them, that they can’t go to other countries preaching their hate, preaching their cult of death."
More than 800 UK citizens are thought to have gone to fight for Islamic State in Iraq and Syria. Around half of them have already returned, and around 130 have been killed, leaving an estimated 270 left.
Lord Campbell said Mr Williamson's comments "are ill-considered and appear to endorse a clear breach of humanitarian law".
"In present circumstances it is not difficult to see that any member of the military that followed his advice could be subjected to court-martial and prosecution," said Lord Campbell.
"The gung-ho opinions that he has expressed undermine the credibility of British armed forces in general and his office in particular."
And Liberal Democrat home affairs spokesman Sir Ed Davey warned that "eliminating" IS foreign fighters would leave the UK with "zero understanding of why these people have decided to go and fight for the most evil group we have seen in modern times and with zero intelligence".
Labour MP John Woodcock said an "insecure" Defence Secretary was "shooting from the hip to mask his inexperience" and "risks endangering the lives of British troops with this fatuous posturing".
Mr Woodcock warned: "If he is not slapped down, any future enemy of Britain could say, 'Why should we respect the Geneva convention on captured British soldiers when the British don't respect it for their own citizens?'"
Asked whether Theresa May backed Mr Williamson's call for Britons who fight for IS to be hunted down and eliminated, the Prime Minister's official spokesman said:
"The Government position on this has been made clear a number of times in recent months, which is that if you travel to Iraq and Syria and if you are fighting with our enemies there, then you make yourself a legitimate target."
The spokesman added: "There are existing powers in relation to foreign fighters who seek to return to the UK.
"They include exclusion orders that allow the UK to cancel an individual's passport.
"In instances where people do return to the UK, we are clear they should face the consequences of their actions, which include an investigation by police and possible prosecution."