diff --git a/esphome/components/esp8266/const.py b/esphome/components/esp8266/const.py
index 7e152ac41c7..bab40174c4f 100644
--- a/esphome/components/esp8266/const.py
+++ b/esphome/components/esp8266/const.py
@@ -37,15 +37,20 @@ def preference_words(value_bytes: int) -> int:
     return (value_bytes + 3) // 4 + 1
 
 
-def preference_slots(value_bytes: int, restore_from_flash: bool) -> int:
-    """How many values of this size fit, given where restore_from_flash sends them."""
+def preference_slots(value_bytes: int, in_flash: bool, restore_from_flash: bool) -> int:
+    """How many values of this size fit where make_preference() puts them."""
     words = preference_words(value_bytes)
-    regions = (
-        (PREFERENCES_FLASH_WORDS,)
-        if restore_from_flash
-        else (PREFERENCES_RTC_NORMAL_WORDS, PREFERENCES_RTC_EBOOT_WORDS)
+    if in_flash or restore_from_flash:
+        store = (
+            PREFERENCES_FLASH_WORDS
+            if restore_from_flash
+            else PREFERENCES_FLASH_WORDS_WITHOUT_RESTORE
+        )
+        return store // words
+    return sum(
+        region // words
+        for region in (PREFERENCES_RTC_NORMAL_WORDS, PREFERENCES_RTC_EBOOT_WORDS)
     )
-    return sum(region // words for region in regions)
 
 
 # esp8266 namespace is already defined by arduino, manually prefix esphome
diff --git a/esphome/components/esp8266/preferences.cpp b/esphome/components/esp8266/preferences.cpp
index e11f1bec022..4af45b7c3d6 100644
--- a/esphome/components/esp8266/preferences.cpp
+++ b/esphome/components/esp8266/preferences.cpp
@@ -27,7 +27,9 @@ static constexpr uint32_t ESP_RTC_USER_MEM_SIZE_BYTES = ESP_RTC_USER_MEM_SIZE_WO
 static constexpr uint32_t RTC_EBOOT_REGION_WORDS = ESP8266_PREFERENCES_RTC_EBOOT_WORDS;
 static constexpr uint32_t RTC_NORMAL_REGION_WORDS = ESP8266_PREFERENCES_RTC_NORMAL_WORDS;
 static constexpr uint32_t PREF_TOTAL_WORDS = RTC_EBOOT_REGION_WORDS + RTC_NORMAL_REGION_WORDS;  // 110
-static_assert(PREF_TOTAL_WORDS <= ESP_RTC_USER_MEM_SIZE_WORDS, "preference regions overflow RTC memory");
+static constexpr uint32_t RTC_CRASH_HANDLER_WORDS = 18;  // Words 110-127, see crash_handler.cpp
+static_assert(PREF_TOTAL_WORDS + RTC_CRASH_HANDLER_WORDS <= ESP_RTC_USER_MEM_SIZE_WORDS,
+              "preference regions overlap the crash handler's RTC words");
 
 // Maximum preference size in words (limited by uint8_t length_words field)
 static constexpr uint32_t MAX_PREFERENCE_WORDS = 255;
@@ -54,7 +56,7 @@ static inline bool esp_rtc_user_mem_write(uint32_t index, uint32_t value) {
   if (index >= ESP_RTC_USER_MEM_SIZE_WORDS) {
     return false;
   }
-  if (index < 32 && s_prevent_write) {
+  if (index < RTC_EBOOT_REGION_WORDS && s_prevent_write) {
     return false;
   }
 
diff --git a/tests/unit_tests/components/esp8266/test_preferences.py b/tests/unit_tests/components/esp8266/test_preferences.py
new file mode 100644
index 00000000000..550dbf58b14
--- /dev/null
+++ b/tests/unit_tests/components/esp8266/test_preferences.py
@@ -0,0 +1,31 @@
+"""The config-time fit rule must match make_preference() in preferences.cpp."""
+
+import pytest
+
+from esphome.components.esp8266.const import preference_slots, preference_words
+
+
+@pytest.mark.parametrize(
+    ("value_bytes", "words"), [(0, 1), (1, 2), (4, 2), (5, 3), (94, 25)]
+)
+def test_preference_words_rounds_up_and_adds_the_checksum(
+    value_bytes: int, words: int
+) -> None:
+    assert preference_words(value_bytes) == words
+
+
+def test_rtc_values_cannot_straddle_the_regions() -> None:
+    # 25 words each: 3 fit in the 78-word region and 1 in the 32-word one
+    assert preference_slots(94, in_flash=False, restore_from_flash=False) == 4
+    # 32 words each: 2 + 1, where 110 // 32 would also say 3
+    assert preference_slots(124, in_flash=False, restore_from_flash=False) == 3
+    # 39 words each: 2 + 0, where 110 // 39 would say 2 as well but the eboot region is skipped
+    assert preference_slots(152, in_flash=False, restore_from_flash=False) == 2
+    # Larger than the biggest region
+    assert preference_slots(400, in_flash=False, restore_from_flash=False) == 0
+
+
+def test_flash_store_size_follows_restore_from_flash() -> None:
+    assert preference_slots(94, in_flash=True, restore_from_flash=True) == 5
+    assert preference_slots(94, in_flash=False, restore_from_flash=True) == 5
+    assert preference_slots(94, in_flash=True, restore_from_flash=False) == 2