Speaking during the annual Aspen Security Forum, Johnson was careful not to mention GOP presidential nominee Donald Trump, but warned that anti-Muslim campaign chatter "is a setback to our homeland security efforts."
"Overheated rhetoric that fans the flames of fear and prejudice has consequences," he said.
Democrats have criticized Trump's campaign for its pledges to block all or some Muslim immigration into the U.S.
Johnson said his agency has endeavored to work with American Muslims to improve intelligence efforts and get advanced warning of potential lone wolf terrorist strikes.
"There is very definitely a role for the public to play in this environment," Johnson said. "The public can and has made a difference through vigilance and awareness.
Johnson is the latest leader in President Barack Obama's administration to counter the image of the United States that Trump delivered last week at his party's convention in Cleveland.
Trump, who is set to visit Colorado Springs on Friday, has used dark imagery to bolster his pledge to "make America safe again." Johnson said despite threats from Islamic State-inspired terrorists and rising racial tensions related to recent police shootings across the nation, he's optimistic.
"In our world good news is no news and nobody seems to be interested in the good news and the good work of Homeland Security employees every day," Johnson said.
Johnson became the fourth director of Homeland Security in 2013, and has worked to calm Americans' fears about terror attacks and undocumented immigrants. His agency handles border security, immigration, airport security, the Secret Service, Coast Guard and customs agents.
Homeland Security has been a key target on the campaign trail for Trump, who has famously promised to build a wall along the U.S.-Mexico border to stop illegal immigrants from entering the country. Trump has also criticized Obama's policies on Syrian refugees, saying accepting the immigrants puts the U.S. at risk of a terror attack.
Johnson has backed Obama administration policies that used executive orders to make it easier for some undocumented immigrants to linger in the United States.
On Wednesday, he focused on confronting homegrown terrorists.
Johnson said the Islamic State group, which has taken over a wide swath of Iraq and Syria, now seeks to "inspire people to stay home and commit terrorist attacks. It's low-risk low cost."
The government can't take on homegrown terrorists alone, he said. Tips from the public are key.
"I think there is a way to channel the sense of anxiety now into a more positive and constructive awareness of how we can support our homeland security law enforcement officials," he said. "There is a role for the public to play."
Johnson's talk kicked off an event that runs through Saturday, highlighting national security concerns. Scheduled to speak this week are National Intelligence director James Clapper, Army Gen. Joseph Votel, head of U.S. Central Command, and CIA boss John Brennan.
The four-day forum is put on by the Aspen Institute and draws a well-heeled crowd to this tony ski town along with current and former leaders of the national security establishment. Tickets to the event run $1,700.
The topics covered vary widely. Johnson's remarks included his view of U.S. race relations.
While the country faces many issues, Johnson said, today's problems aren't like the race issues of decades past.
"My great-grandfather, my grandparents and my parents grew up with Jim Crow where they were second-class citizens in law and in fact," Johnson said.
Now, he said, efforts including enhanced community policing may be sufficient to deal with strife.
"I am optimistic and I take the long view."
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