Under Cameron's guidelines, ministers will not be able to campaign for Britain to leave the EU until after negotiations have been completed, warning frontbenchers not to "undermine" his efforts to secure a deal with other member states.
The PM's letter, sent to the frontbench, also explains that anti-EU ministers will be barred from supporting a Brexit vote from the dispatch box, however it hinted that they would be allowed speak out against the government's position from the backbench.
Although Cameron hasn't ruled out campaigning for a Brexit, he has said his preferred choice is for the UK to remain inside a reformed EU. He also noted that he won't make up his mind until negotiations with European counterparts have been completed.
PM has written to ministers setting out collective responsibility guidance on the issue of UK membership of the EU: https://t.co/SUhf599Kpf— No. 10 Press Office (@Number10press) January 12, 2016
On top of restrictions on ministers, the prime minister has also made it clear that the civil service will be fully behind the government's decision, which is expected to be in favor of remaining in the bloc.
"It will not be appropriate or permissible for the civil service or individual civil servants to support ministers who opposed the Government's official position," the letter states.
'One Rule for Them and Another for the Rest'
Despite Cameron allowing for ministers to express their own views over the EU debate, former environment minister Owen Paterson, who is a leading member of the Vote Leave group, says the new ground rules will severely restrict the rights of Euroskeptic ministers to campaign for a Brexit.
"It's welcome that ministers who want to campaign to take back control from the EU will be able to do so without resigning, but it's increasingly clear that it'll be one rule for those who want to stay in the EU at all costs, and another rule for the rest," Paterson said.
"Ministers who wish to extol the virtues of the EU have been given a green light to do so already, while those who want to take back control are currently gagged… It looks like the government is focusing its energies on gearing up the full weight of the Whitehall machine to campaign to keep us in the EU rather than on bringing powers back from Brussels."
The prime minister is desperate to avoid the damaging party splits that dogged former PM Sir John Major's time in office, with reports suggesting two-thirds of MPs are leaning towards voting in favor of a Brexit.
A problem in the so called EU negotiations is that the EU leaders believe Cameron will never #brexit— Lord Ashcroft (@LordAshcroft) December 18, 2015
In his letter he called for party unity regardless of the differences in opinion on the matter of EU membership.
"Throughout this period, and in its aftermath, we will continue to have responsibility for governing the country and serving the public who elected us. This can only be done effectively if we remain, despite differences on this one issue, a united, harmonious, mutually respectful team."