The Catholic Church and the state were for centuries virtually indistinguishable in France but the 1789 Revolution and 19th century modernisation saw the two formally separated by a 1905 law.
Macron, who prides himself on tackling difficult issues head-on, told a meeting of bishops on Monday that he hoped to repair relations with the Church through a "dialogue of truth".
"A president of the French republic who takes no interest in the Church and its Catholics would be failing in his duty," he said.
Former socialist prime minister Manuel Valls, who backed Macron for president in 2017, tweeted that "secularism is France".
La laïcité c’est la France, et elle n’a qu’un seul fondement : la loi de 1905, celle de la séparation des Eglises et de l’Etat. La loi de 1905, toute la loi, rien que la loi.Manuel Valls (@manuelvalls) April 9, 2018
"Secularism is the jewel in our crown. That is what a president of the republic should be defending," newly-installed Socialist Party leader Olivier Faure said in a tweet.
Jean-Luc Mélenchon, lead of the left-wing France Insoumise (France Unbowed) party, said Macron's remarks were "irresponsible".
"Macron in full-on metaphysical delirium. Outrageous. One expects a president, one gets a little priest," Mélenchon said in a tweet.
Interior Minister Gerard Collomb, who is responsible for government relations with religious groups, said Macron's remarks reflected the need for greater spiritual awareness and did not undermine France's secular traditions.
"What he is saying is that for human beings, there is not only the material world but also the search for absolute values, for spirituality, to find meaning in life," he said.
"It is perhaps a new tone but in no way does it break with the great tradition of secularism."
Opinion polls show the French roughly split between believers and non-believers while the role and place of religion in the country remains sensitive.