We study the nucleon electromagnetic form factors (EM FFs) using a recently developed method combining chiral effective field theory (χ EFT) and dispersion analysis. The spectral functions on the two-pion cut at t > 4M 2 π are constructed using the elastic unitarity relation and an N/D representation. χ EFT is used to calculate the real functions J 1 ± (t) = f 1 ± (t)/F π (t) (ratios of the complex ππ → NN partial-wave amplitudes and the timelike pion FF), which are free of ππ rescattering. Rescattering effects are included through the empirical timelike pion FF |F π (t)| 2 . The method allows us to compute the isovector EM spectral functions up to t ∼ 1 GeV 2 with controlled accuracy (leading order, next-to-leading order, and partial next-to-next-to-leading order). With the spectral functions we calculate the isovector nucleon EM FFs and their derivatives at t = 0 (EM radii, moments) using subtracted dispersion relations. We predict the values of higher FF derivatives, which are not affected by higher-order chiral corrections and are obtained almost parameter-free in our approach, and explain their collective behavior. We estimate the individual proton and neutron FFs by adding an empirical parametrization of the isoscalar sector. Excellent agreement with the present low-Q 2 FF data is achieved up to ∼0.5 GeV 2 for G E , and up to ∼0.2 GeV 2 for G M . Our results can be used to guide the analysis of low-Q 2 elastic scattering data and the extraction of the proton charge radius.