Key points The two classes of principal neurons in the mammalian main olfactory bulb, mitral and tufted cells, respond with different firing latencies and rates to afferent‐evoked input; how these differences in activity arise is incompletely understood. Tufted cells receive stronger afferent‐evoked excitation than mitral cells, but this difference alone is insufficient to account for the greater afferent‐evoked firing in tufted versus mitral cells. Mitral and tufted cells exhibit significant intrinsic functional differences; compared to mitral cells, tufted cells fire action potentials with shorter durations and faster afterhyperpolarizations and exhibit twofold greater firing rate–current curve gains and peak rates. Tufted cells exhibit diverse firing modes, including tonic firing and irregular stuttering, and on average fire more irregularly than mitral cells. Collectively, stronger afferent excitation, greater intrinsic excitability and more irregular firing in tufted cells combine to drive distinct responses of mitral and tufted cells to sensory input. Abstract Mitral and tufted cells, the two classes of principal neurons in the mammalian main olfactory bulb, exhibit morphological differences but remain widely viewed as functionally equivalent. Results from several recent studies, however, suggest that these two cell classes may encode complementary olfactory information in their distinct patterns of afferent‐evoked activity. To understand how these differences in activity arise, we have performed the first systematic comparison of synaptic and intrinsic properties between mitral and tufted cells. Consistent with previous studies, we found that tufted cells fire with higher probability and rates and shorter latencies than mitral cells in response to physiological afferent stimulation. This stronger response of tufted cells could be partially attributed to synaptic differences, as tufted cells received stronger afferent‐evoked excitation than mitral cells. However, differences in intrinsic excitability also contributed to the differences between mitral and tufted cell activity. Compared to mitral cells, tufted cells exhibited twofold greater excitability and peak instantaneous firing rates. These differences in excitability probably arise from differential expression of voltage‐gated potassium currents, as tufted cells exhibited faster action potential repolarization and afterhyperpolarizations than mitral cells. Surprisingly, mitral and tufted cells also showed firing mode differences. While both cell classes exhibited regular firing and irregular stuttering of action potential clusters, tufted cells demonstrated a greater propensity to stutter than mitral cells. Collectively, stronger afferent‐evoked excitation, greater intrinsic excitability and more irregular firing in tufted cells can combine to drive distinct responses of mitral and tufted cells to afferent‐evoked input.