diff --git a/r/R/util.R b/r/R/util.R
index c63e1ee5459..cb98358b432 100644
--- a/r/R/util.R
+++ b/r/R/util.R
@@ -196,6 +196,18 @@ repeat_value_as_array <- function(object, n) {
 }
 
 handle_csv_read_error <- function(msg, call, schema) {
+  if (grepl("conversion error to null", msg)) {
+    msg <- c(
+      msg,
+      i = paste(
+        "Column type was inferred as null because the first block of data",
+        "contained only missing values. See `?csv_read_options` for how to",
+        "set a smaller value."
+      )
+    )
+    abort(msg, call = call)
+  }
+
   if (grepl("conversion error", msg) && inherits(schema, "Schema")) {
     msg <- c(
       msg,
diff --git a/r/tests/testthat/test-dataset-csv.R b/r/tests/testthat/test-dataset-csv.R
index 749d1672ac5..5cf8e23b097 100644
--- a/r/tests/testthat/test-dataset-csv.R
+++ b/r/tests/testthat/test-dataset-csv.R
@@ -711,3 +711,21 @@ test_that("open_dataset() with `decimal_point` argument", {
     tibble(x = 1.2, y = "c")
   )
 })
+
+test_that("more informative error when column inferred as null due to sparse data (GH-35806)", {
+  tf <- tempfile()
+  on.exit(unlink(tf))
+
+  writeLines(c("x,y", paste0(1:100, ",")), tf)
+  write("101,foo", tf, append = TRUE)
+
+  expect_error(
+    open_dataset(
+      tf,
+      format = "csv",
+      read_options = csv_read_options(block_size = 100L)
+    ) |>
+      collect(),
+    "inferred as null"
+  )
+})