diff --git a/CHANGES b/CHANGES
index b619125c9f..d066845439 100644
--- a/CHANGES
+++ b/CHANGES
@@ -1,3 +1,27 @@
+3707.	[bug]		irs_resconf_load now returns ISC_R_FILENOTFOUND
+			on a missing resolv.conf file and initializes the
+			structure as if it had been configured with:
+
+				nameserver ::1
+				nameserver 127.0.0.1
+
+			Note: Callers will need to be updated to treat
+			ISC_R_FILENOTFOUND as a qualified success or else
+			they will leak memory. The following code fragment
+			will work with both only and new versions without
+			changing the behaviour of the existing code.
+
+			resconf = NULL;
+			result = irs_resconf_load(mctx, "/etc/resolv.conf",
+						  &resconf);
+			if (result != ISC_SUCCESS) {
+				if (resconf != NULL)
+					irs_resconf_destroy(&resconf);
+				....
+			}
+
+			[RT #35194]
+
 3706.	[contrib]	queryperf: Fixed a possible integer overflow when
 			printing results. [RT #35182]
 
diff --git a/lib/irs/include/irs/resconf.h b/lib/irs/include/irs/resconf.h
index 78c87d5166..c6c6e851bc 100644
--- a/lib/irs/include/irs/resconf.h
+++ b/lib/irs/include/irs/resconf.h
@@ -46,7 +46,12 @@ isc_result_t
 irs_resconf_load(isc_mem_t *mctx, const char *filename, irs_resconf_t **confp);
 /*%<
  * Load the resolver configuration file 'filename' in the "resolv.conf" format,
- * and create a new irs_resconf_t object from the configuration.
+ * and create a new irs_resconf_t object from the configuration.  If the file
+ * is not found ISC_R_FILENOTFOUND is returned with the structure initialized
+ * as if file contained only:
+ *
+ *	nameserver ::1
+ *	nameserver 127.0.0.1
  *
  * Notes:
  *
@@ -55,6 +60,11 @@ irs_resconf_load(isc_mem_t *mctx, const char *filename, irs_resconf_t **confp);
  *	In addition, 'sortlist' is not actually effective; it's parsed, but
  *	the application cannot use the configuration.
  *
+ * Returns:
+ * \li	ISC_R_SUCCESS on success
+ * \li  ISC_R_FILENOTFOUND if the file was not found. *confp will be valid.
+ * \li  other on error.
+ *
  * Requires:
  *
  *\li	'mctx' is a valid memory context.
diff --git a/lib/irs/resconf.c b/lib/irs/resconf.c
index 15a46baf3f..29cfb75fef 100644
--- a/lib/irs/resconf.c
+++ b/lib/irs/resconf.c
@@ -507,45 +507,50 @@ irs_resconf_load(isc_mem_t *mctx, const char *filename, irs_resconf_t **confp)
 		conf->search[i] = NULL;
 
 	errno = 0;
-	if ((fp = fopen(filename, "r")) == NULL) {
-		isc_mem_put(mctx, conf, sizeof(*conf));
-		return (ISC_R_INVALIDFILE);
-	}
-
-	ret = ISC_R_SUCCESS;
-	do {
-		stopchar = getword(fp, word, sizeof(word));
-		if (stopchar == EOF) {
-			rval = ISC_R_SUCCESS;
-			POST(rval);
-			break;
-		}
-
-		if (strlen(word) == 0U)
-			rval = ISC_R_SUCCESS;
-		else if (strcmp(word, "nameserver") == 0)
-			rval = resconf_parsenameserver(conf, fp);
-		else if (strcmp(word, "domain") == 0)
-			rval = resconf_parsedomain(conf, fp);
-		else if (strcmp(word, "search") == 0)
-			rval = resconf_parsesearch(conf, fp);
-		else if (strcmp(word, "sortlist") == 0)
-			rval = resconf_parsesortlist(conf, fp);
-		else if (strcmp(word, "options") == 0)
-			rval = resconf_parseoption(conf, fp);
-		else {
-			/* unrecognised word. Ignore entire line */
-			rval = ISC_R_SUCCESS;
-			stopchar = eatline(fp);
+	if ((fp = fopen(filename, "r")) != NULL) {
+		ret = ISC_R_SUCCESS;
+		do {
+			stopchar = getword(fp, word, sizeof(word));
 			if (stopchar == EOF) {
+				rval = ISC_R_SUCCESS;
+				POST(rval);
 				break;
 			}
-		}
-		if (ret == ISC_R_SUCCESS && rval != ISC_R_SUCCESS)
-			ret = rval;
-	} while (1);
 
-	fclose(fp);
+			if (strlen(word) == 0U)
+				rval = ISC_R_SUCCESS;
+			else if (strcmp(word, "nameserver") == 0)
+				rval = resconf_parsenameserver(conf, fp);
+			else if (strcmp(word, "domain") == 0)
+				rval = resconf_parsedomain(conf, fp);
+			else if (strcmp(word, "search") == 0)
+				rval = resconf_parsesearch(conf, fp);
+			else if (strcmp(word, "sortlist") == 0)
+				rval = resconf_parsesortlist(conf, fp);
+			else if (strcmp(word, "options") == 0)
+				rval = resconf_parseoption(conf, fp);
+			else {
+				/* unrecognised word. Ignore entire line */
+				rval = ISC_R_SUCCESS;
+				stopchar = eatline(fp);
+				if (stopchar == EOF) {
+					break;
+				}
+			}
+			if (ret == ISC_R_SUCCESS && rval != ISC_R_SUCCESS)
+				ret = rval;
+		} while (1);
+
+		fclose(fp);
+	} else {
+		switch (errno) {
+		case ENOENT:
+			break;
+		default:
+			isc_mem_put(mctx, conf, sizeof(*conf));
+			return (ISC_R_INVALIDFILE);
+		}
+	}
 
 	/* If we don't find a nameserver fall back to localhost */
 	if (conf->numns == 0) {
@@ -575,8 +580,11 @@ irs_resconf_load(isc_mem_t *mctx, const char *filename, irs_resconf_t **confp)
 
 	if (ret != ISC_R_SUCCESS)
 		irs_resconf_destroy(&conf);
-	else
+	else {
+		if (fp == NULL)
+			ret = ISC_R_FILENOTFOUND;
 		*confp = conf;
+	}
 
 	return (ret);
 }
diff --git a/lib/samples/resolve.c b/lib/samples/resolve.c
index 95475ebb21..278e0e292d 100644
--- a/lib/samples/resolve.c
+++ b/lib/samples/resolve.c
@@ -401,7 +401,7 @@ main(int argc, char *argv[]) {
 		isc_sockaddrlist_t *nameservers;
 
 		result = irs_resconf_load(mctx, "/etc/resolv.conf", &resconf);
-		if (result != ISC_R_SUCCESS) {
+		if (result != ISC_R_SUCCESS && result != ISC_R_FILENOTFOUND) {
 			fprintf(stderr, "irs_resconf_load failed: %d\n",
 				result);
 			exit(1);