diff --git a/R/paginate.R b/R/paginate.R
index cb84db3b..a0f6482c 100644
--- a/R/paginate.R
+++ b/R/paginate.R
@@ -28,6 +28,8 @@
 #'     * `next_url` for `paginate_next_url()`.
 #'     * `next_token` for `paginate_next_token()`.
 #'
+#' @param required_fields An optional character vector that describes which
+#'   fields are required in the list returned by `parse_resp()`.
 #' @param n_pages An optional function that extracts the total number of pages, improving the
 #'   automatically generated progress bar. It has two arguments:
 #'
@@ -63,19 +65,37 @@
 req_paginate <- function(req,
                          next_request,
                          parse_resp = NULL,
+                         required_fields = NULL,
                          n_pages = NULL) {
   check_request(req)
   check_function2(next_request, args = c("req", "parsed"))
   check_function2(parse_resp, args = "resp", allow_null = TRUE)
   parse_resp <- parse_resp %||% function(resp) list(data = resp)
+  check_character(required_fields, allow_null = TRUE)
+  required_fields <- union(required_fields, "data")
   check_function2(n_pages, args = "parsed", allow_null = TRUE)
   n_pages <- n_pages %||% function(parsed) Inf
 
+  wrapped_parse_resp <- function(resp) {
+    out <- parse_resp(resp)
+    if (!is.list(out)) {
+      cli::cli_abort("{.fun parse_resp} must return a list, not {.obj_type_friendly {out}}.")
+    }
+
+    missing_fields <- setdiff(required_fields, names2(out))
+    if (!is_empty(missing_fields)) {
+      cli::cli_abort(c("The list returned by {.code parse_resp(resp)} is missing the field{?s} {.field {missing_fields}}."))
+    }
+
+    out
+  }
+
   req_policies(
     req,
     paginate = list(
       next_request = next_request,
-      parse_resp = parse_resp,
+      parse_resp = wrapped_parse_resp,
+      required_fields = required_fields,
       n_pages = n_pages
     )
   )
@@ -205,6 +225,7 @@ req_paginate_next_url <- function(req,
     req,
     next_request,
     parse_resp = parse_resp,
+    required_fields = "next_url",
     n_pages = n_pages
   )
 }
@@ -237,6 +258,7 @@ req_paginate_token <- function(req,
     req,
     next_request,
     parse_resp = parse_resp,
+    required_fields = "next_token",
     n_pages = n_pages
   )
 }
diff --git a/tests/testthat/_snaps/paginate.md b/tests/testthat/_snaps/paginate.md
index a8dedbc4..6ba546f0 100644
--- a/tests/testthat/_snaps/paginate.md
+++ b/tests/testthat/_snaps/paginate.md
@@ -130,6 +130,32 @@
       Error in `paginate_req_perform()`:
       ! `progress` must be a bool, a string, or a list, not the number -1.
 
+# parse_resp() produces a good error message
+
+    Code
+      req_not_a_list$policies$paginate$parse_resp(resp)
+    Condition
+      Error in `req_not_a_list$policies$paginate$parse_resp()`:
+      ! `parse_resp()` must return a list, not a string.
+    Code
+      req_missing_1_field$policies$paginate$parse_resp(resp)
+    Condition
+      Error in `req_missing_1_field$policies$paginate$parse_resp()`:
+      ! The list returned by `parse_resp(resp)` is missing the field next_url.
+    Code
+      req_missing_2_field$policies$paginate$parse_resp(resp)
+    Condition
+      Error in `req_missing_2_field$policies$paginate$parse_resp()`:
+      ! The list returned by `parse_resp(resp)` is missing the fields next_url and data.
+
+---
+
+    Code
+      paginate_req_perform(req, max_pages = 2)
+    Condition
+      Error in `parse_resp()`:
+      ! The list returned by `parse_resp(resp)` is missing the field next_token.
+
 # paginate_req_perform() handles error in `parse_resp()`
 
     Code
diff --git a/tests/testthat/test-paginate.R b/tests/testthat/test-paginate.R
index 392782fe..c6a3103f 100644
--- a/tests/testthat/test-paginate.R
+++ b/tests/testthat/test-paginate.R
@@ -55,7 +55,7 @@ test_that("req_paginate_next_url() can paginate", {
   req1 <- request("https://pokeapi.co/api/v2/pokemon") %>%
     req_url_query(limit = 11) %>%
     req_paginate_next_url(
-      parse_resp = function(resp) list(next_url = resp_body_json(resp)[["next"]])
+      parse_resp = function(resp) list(data = "a", next_url = resp_body_json(resp)[["next"]])
     )
 
   resp <- req_perform(req1)
@@ -208,6 +208,35 @@ test_that("paginate_req_perform() works if there is only one page", {
   expect_length(responses, 1)
 })
 
+test_that("parse_resp() produces a good error message", {
+  req_not_a_list <- request("https://pokeapi.co/api/v2/pokemon") %>%
+    req_paginate_next_url(parse_resp = function(resp) "a")
+  req_missing_1_field <- request("https://pokeapi.co/api/v2/pokemon") %>%
+    req_paginate_next_url(parse_resp = function(resp) list(data = "a"))
+  req_missing_2_field <- request("https://pokeapi.co/api/v2/pokemon") %>%
+    req_paginate_next_url(parse_resp = function(resp) list(x = "a"))
+  resp <- response()
+
+  expect_snapshot(error = TRUE, {
+    req_not_a_list$policies$paginate$parse_resp(resp)
+    req_missing_1_field$policies$paginate$parse_resp(resp)
+    req_missing_2_field$policies$paginate$parse_resp(resp)
+  })
+
+  # The error call is helpful
+  req <- request_pagination_test(
+    parse_resp = function(resp) {
+      parsed <- resp_body_json(resp)
+
+      list(parsed$my_next_token, data = parsed)
+    }
+  )
+
+  expect_snapshot(error = TRUE, {
+    paginate_req_perform(req, max_pages = 2)
+  })
+})
+
 test_that("paginate_req_perform() handles error in `parse_resp()`", {
   req <- request_pagination_test(
     parse_resp = function(resp) {