“Apologists” for those who commit acts of terrorism are partly responsible for the violence, Philip Hammond will say.
Security services have been criticised over their handling of Mohammed Emwazi – known as “Jihadi John”.
But in a speech later the foreign secretary will praise the “brilliance” of Britain’s intelligence officers.
He will also say ministers must act “decisively” in debates about powers given to the security services so they can “get on” with keeping the UK safe.
Speaking at the Royal United Services Institute in London, Mr Hammond will say: “We are absolutely clear; the responsibility for acts of terror rests with those who commit them.
“But a huge burden of responsibility also lies with those who act as apologists for them.”
BBC security correspondent Gordon Corera said critics of the security services said they “could have done more” to prevent Emwazi travelling to the Middle East.
Cage, an advocacy group for those “impacted by the War on Terror”, has said MI5 played a role in the radicalisation of Emwazi.
Its research director Asim Qureshi told the BBC “harassment” by intelligence officers did not make Emwazi into a killer, but he said it was a factor in making him feel he “didn’t belong in the UK anymore”.
Who is Mohammed Emwazi?
Emwazi was born in Kuwait in 1988 and came to the UK at the age of six.
He went to school in London and graduated from the University of Westminster in 2009 with a degree in computing.
He came to the attention of security services in the same year and was deported as he tried to enter Tanzania, though the circumstances of this are disputed.
He then spent two spells in Kuwait, but Cage said he was prevented from returning to the country after a trip to Britain.
He later went missing, and police told his family he had gone to Syria.
He has subsequently been identified as the militant in the August 2014 video showing the murder of US journalist James Foley, and in several similar videos showing the beheading of hostages.
Also in his speech, Mr Hammond will say Britain must maintain a “highly effective, secret capability” to identify, monitor and act against terrorist threats.
“The sheer number and range of cases, old and new, amounts to the greatest challenge to our collective security for decades and places unprecedented demands on those charged with keeping us safe,” he will say.
“We must respond decisively and positively to the public and parliamentary debate about the powers required by our intelligence agencies to do their job in a changed technological environment – and in doing so draw a line under that debate so that the agencies can get on with the job of keeping this country safe.”
Mr Hammond will say the emergence of militant groups such as Islamic State and Boko Haram show the “pace” with which threats to UK security are “evolving”.
“It is only thanks to the dedication, and in many cases the brilliance, of our intelligence officers that we have succeeded to detect and contain these threats,” he will add.
He will also accuse Russian President Vladimir Putin of “subverting” the system of rules which “keeps the peace between nations” by annexing Crimea and “now using Russian troops to destabilise eastern Ukraine”.
Russia denies having troops in Ukraine, saying that any Russian soldiers among the rebels are “volunteers”.