The tensions over policing and crime come when, for the first time in a generation, unusual political forces have aligned and the nation appears on the verge of relaxing tough criminal sentencing laws. Liberals and conservatives now seem to agree that 1980's-era anti-drug laws boosted U.S. prison populations too much, with the burden falling disproportionately on minority communities.
Some law enforcement officials, including Comey, are raising concerns that a spike in crime -- or at least the perception that the recent era of historically low crime rates is at risk -- could hurt criminal justice reforms efforts.
The crime spike is showing up in a variety of cities big and small, while others have avoided the same. Cleveland and Milwaukee have blown past the number of murders reported in 2014, with more than two months left in the year. Dallas and Tampa in recent weeks were on pace to surpass 2014 murder totals. Meanwhile, other cities, including New York, haven't seen similar increases.
At the same time, a number of high-profile police shooting incidents, many caught on ubiquitous camera phones, have given rise to protests over policing tactics that critics call heavy-handed. In some cities, police officers privately report holding back on making stops for fear of ending up the next YouTube "bad cop" sensation. They call it the Ferguson effect.
These are among the issues facing the nation's top local and federal law enforcement officials meeting in Chicago this week. President Barack Obama and Attorney General Loretta Lynch are scheduled to address the gathering of the International Association of Chiefs of Police.
As if to underscore the roiling controversies hanging over policing in America, on Saturday hundreds of protesters staged what they called an "I Shocked the Sheriff" Counter-Conference outside the Chicago convention hall hosting the IACP meetings. Police made dozens of arrests when protesters blocked intersections.
Comey waded into the thorny issues at play in a speech Friday at the University of Chicago Law School, his alma mater. He has expressed worry about the spike in the number murders in some cities, and for the first time said it could be at least partly linked to what he called a "chill wind" police are facing in the wake of Ferguson.
"Far more people are being killed in America's cities this year than in many years -- and let's be clear: far more people of color are being killed in America's cities this year. And it's not the cops doing the killing," Comey said.
The FBI chief repeatedly used the phrase "all lives matter" in various contexts during his discussion led by Ruby Garrett, editor of the law school's Legal Forum and president of the Black Law Students Association. The phrase has drawn controversy because some view it as a response to the advent of the Black Lives Matter movement. The two spoke before a mostly white student audience.
The provocative remarks expanded on themes Comey first broached in a 2014 speech at Georgetown University, where he acknowledged racial biases were at times to blame for "lazy mental shortcuts" that lead to more police stops of young black men.
But in Friday's speech, and again Sunday, he said he was trying to start a conversation about whether the pendulum has swung too far.
"In today's YouTube world, are officers reluctant to get out of their cars and do the work that controls violent crime? Are officers answering 911 calls but avoiding the informal contact that keeps bad guys from standing around, especially with guns?" he asked in his Friday remarks. "I don't know whether this explains it entirely, but I do have a strong sense that some part of the explanation is a chill wind blowing through American law enforcement over the last year. And that wind is surely changing behavior."
Ray Kelly, the former commissioner of the New York Police Department, said Monday that police are no longer "taking the initiative," which he said accounts for some of the rise in crime.
"I commend Jim Comey for telling it like it is," Kelly told CNN's Wolf Blitzer on "The Situation Room." "Officers are not engaging in proactive policing, not engaging in the levels they engaged in the recent past."
White House press secretary Josh Earnest said Monday there was no evidence that police officers were "shirking" their duties given increased scrutiny on law enforcement, seeming to rebut FBI Director James Comey's assertion last week.
"The available evidence at this point does not support the notion that law enforcement officers are shying away from fulfilling their responsibilities," Earnest said at the daily briefing.
He cited national law enforcement leaders saying that there's little proof that police forces are relaxing their practices after high profile incidents of videotaped police brutality.
"The evidence we've seen so far doesn't support the contention that law enforcement officials are somehow shirking their responsibility, and in fact you've seen law enforcement leaders across the country indicating that's not what's taking place," he said.
Comey appeared to soften his tone in his remarks in Chicago on Monday to International Association of Chiefs of Police convention in Chicago.
Comey noted the discordant tones of the social media hashtags #BlackLivesMatter and #PoliceLivesMatter, which he said was pitting police against critics who believe black communities are bearing the brunt of heavy-handed police tactics.
This, Comey said, "is a terrible place for us to be."
He urged police chiefs to help the FBI gather better data about of officer-involved shootings and other use-of-force incidents.
"We need to figure out what's happening," Comey said, adding that he also wants data on assaults on cops.
To be sure, violent crime remains at historic lows.
Even in cities where dozens of shootings in a weekend regularly make national headlines, violent crime rates were far higher 20 years ago. Chicago has recorded over 400 murders this year, but that's well short of the more than 900 common in the early 1990s. Police in Washington, D.C., which recorded nearly 400 murders in 1996, are facing public pressure because of 124 killings this year, an increase from 88 in 2012.
Comey's cautious endorsement of the Ferguson Effect may be welcomed by some in policing, but many other police chiefs disagree. To do so, some say privately, would admit that their officers aren't doing their jobs. Many other chiefs blame a rise in synthetic drugs and other discrete causes for crime.
New York City Police Commissioner William Bratton says he's not seeing the so-called Ferguson effect in his city. There was a brief period last winter, in the wake of the ambush murder of two officers, that arrests dipped before returning to normal levels.
In an interview with CNN, Bratton said he believes what's happening around the country is part of the "evolution of policing" which will eventually make officers better.
"A cop sitting in his car is not what a cop should be," Bratton said.
Groups that grew out of the Ferguson protests dispute that crime rates have any link to their efforts to shine a light on what they believe is widespread problem of excessive use of force.
The nature of U.S. policing, with more than 12,000 local police departments, makes it difficult to gather statistics on police shootings. Because not all police departments collect and report such numbers, no national count exists.
The president and attorney general are both expected to their pitch for criminal justice reform to the gathering of police.
But both are likely to give remarks generally supportive of police.
That's a message that likely will go over well inside the convention hall in Chicago. Outside, the jury remains out.