Evolutionary psychology seeks to identify and understand human psychological traits that have evolved in much the same way as biological traits, through adaptation to environmental cues. Furthermore, it tends toward viewing the vast majority of psychological traits, certainly the most important ones, as the result of past adaptions, which has generated significant controversy and criticism from competing fields. These criticisms include disputes about the testability of evolutionary hypotheses, cognitive assumptions such as massive modularity, vagueness stemming from assumptions about the environment that leads to evolutionary adaptation, the importance of non-genetic and non-adaptive explanations, as well as political and ethical issues in the field itself.

Evolutionary psychologists contend that a number of the criticisms against it are straw men, based on an incorrect nature versus nurture dichotomy, and/or based on misunderstandings of the discipline. In addition, some defenders of evolutionary psychology assert that critics of the discipline base their criticisms on a priori political assumptions, such as those associated with Marxism.

The history of the debate from a critic's perspective is detailed by Gannon (2002). Critics of evolutionary psychology include the philosophers of science David Buller (author of Adapting Minds), Robert C. Richardson (author of Evolutionary Psychology as Maladapted Psychology), and Brendan Wallace (author of Getting Darwin Wrong: Why Evolutionary Psychology Won't Work). Other critics include neurobiologists like Steven Rose (who edited Alas, Poor Darwin: Arguments against Evolutionary Psychology), biological anthropologists like Jonathan Marks, and social anthropologists like Tim Ingold and Marshall Sahlins.

Responses defending evolutionary psychology against critics have been published in books including Segerstråle's Defenders of the Truth: The Battle for Science in the Sociobiology Debate and Beyond (2000), Barkow's Missing the Revolution: Darwinism for Social Scientists (2005), and Alcock's The Triumph of Sociobiology (2001). Other responses to critics include Confer et al. (2010), Tooby and Cosmides (2005), and Hagen (2005). Furthermore, in one frequently quoted rebuttal of most such critics, psychologist Anne Campbell posited that such people merely believe "evolution stops at the neck".

Evolutionary psychologists have postulated that the mind is composed of cognitive modules specialized to perform specific tasks. Evolutionary psychologists have theorized that these specialized modules enabled our ancestors to react quickly and effectively to environmental challenges. As a result, domain-specific modules would have been selected for, whereas broad general-purpose cognitive mechanisms that worked more slowly would have been eliminated in the course of evolution.

A number of cognitive scientists have criticized the modularity hypothesis, citing neurological evidence of brain plasticity and changes in neural networks in response to environmental stimuli and personal experiences. Steven Quartz and Terry Sejnowski, for example, have argued that the view of the brain as a collection of specialized circuits, each chosen by natural selection and built according to a "genetic blueprint", is contradicted by evidence that cortical development is flexible and that areas of the brain can take on different functions. Neurobiological research does not support the assumption by evolutionary psychologists that higher-level systems in the neocortex responsible for complex functions are massively modular. Peters (2013) cites neurological research showing that higher-order neocortical areas can become functionally specialized by way of synaptic plasticity and the experience-dependent changes that take place at the synapse during learning and memory. As a result of experience and learning processes the developed brain can look modular although it is not necessarily innately modular. However, Klasios (2014) responds to Peters' critique.

Another criticism is that there is little empirical support in favor of the domain-specific theory. Leading evolutionary psychologists Leda Cosmides and John Tooby have found that performance on the selection task is content-dependent: People find it easier to detect violations of "if-then" rules when the rules can be interpreted as cheating on a social contract. From this Cosmides and Tooby and other evolutionary psychologists concluded that the mind consisted of domain-specific, context-sensitive modules (including a cheater-detection module). Critics have suggested that Cosmides and Tooby use untested evolutionary assumptions to eliminate rival reasoning theories and that their conclusions contain inferential errors. Davies et al., for example, have argued that Cosmides and Tooby did not succeed in eliminating the general-purpose theory because the adapted Wason selection task they used tested only one specific aspect of deductive reasoning and failed to examine other general-purpose reasoning mechanisms (e.g., reasoning based on syllogistic logic, predicate logic, modal logic, and inductive logic etc.). Furthermore, Cosmides and Tooby use rules that incorrectly represent genuine social exchange situations. Specifically, they posit that someone who received a benefit and does not pay the cost is cheating. However, in real-life social exchange situations people can benefit and not pay without cheating (as in the case of receiving gifts or benefiting from charity).

Some critics have suggested that our genes cannot hold the information to encode the brain and all its assumed modules. Humans share a significant portion of their genome with other species and have corresponding DNA sequences so that the remaining genes must contain instructions for building specialized circuits that are absent in other mammals.