"What is striking is the catastrophic incompetence of our security services," said Ivan Zhdanov, the former head of late opposition leader Alexei Navalny's Anti-Corruption Foundation.
For Putin, a former Soviet spy and one-time head of the FSB security agency, accusations of an intelligence failure could sting.
He came to power on the final day of 1999 promising Russia security as rebel insurgents launched a spate of attacks amid war in Chechnya.
Putin's first years as president saw militants storm a Moscow theatre, taking more than 900 people hostage, and the Beslan school siege -- in which more than 300 people, mostly children, were killed.
After that, he chipped away at civil liberties and launched an escalating crackdown against his opponents, which he justified by the need to stamp out the terrorist threat.
"For decades we have been told that the curtailment of our rights is necessary for security," Zhdanov said in a post on Telegram over the weekend.
"But the terrorist attacks do not stop, and the FSB is busy with everything except its direct responsibilities " killing their political opponents, spying on citizens and prosecuting people who are against the war.
Russian officials are yet to comment on Islamic State (IS) claiming responsibility for the concert hall attack, which killed more than 130."